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Acknowledgements: EFSA and ECDC wish to thank the members of the Scientific Network for
Zoonoses Monitoring Data (EFSA) and the Food- and Waterborne Diseases and Zoonoses Network
(ECDC) who provided the data and reviewed the report and the members of the Scientific Network for
Zoonoses Monitoring Data, for their endorsement of this scientific output. Also, the contribution of
EFSA staff members: Pierre-Alexandre Belil, Beatriz Guerra, Anca-Violeta Stoicescu, Kenneth
Mulligan, Krisztina Nagy and Mirena Ivanova, the contributions of ECDC staff member: Therese
Westrell, and the contributions of EFSAs contractor: Christopher Teale (Animal and Plant Health
Laboratories Agency United Kingdom), for the support provided to this scientific output.
Amendment: An editorial correction was carried out that does not materially affect the contents or
outcome of this scientific output: O4 has been replaced by O:9 on pages 12 and 13. To avoid
confusion, the older version has been removed from the EFSA Journal, but is available on request, as
is a version showing all the changes made.
Suggested citation: EFSA (European Food Safety Authority) and ECDC (European Centre for
Disease Prevention and Control), 2016. The European Union summary report on antimicrobial
resistance in zoonotic and indicator bacteria from humans, animals and food in 2014. EFSA Journal
2016;14(2):4380, 207 pp. doi:10.2903/j.efsa.2016.4380
ISSN: 1831-4732
European Food Safety Authority and European Centre for Disease Prevention and Control, 2016
Reproduction is authorised provided the source is acknowledged.
Summary
Highlights
Zoonoses are infections that are transmissible between animals and humans. Infections can be
acquired directly from animals, via environmental exposure or through the ingestion of contaminated
foodstuffs. The severity of these diseases in humans can vary from mild symptoms to life-threatening
conditions. Zoonotic bacteria that are resistant to antimicrobials are of particular concern, as they
might compromise the effective treatment of infections in humans. Data from the EU Member States
(MSs) are collected and analysed in order to monitor the occurrence of antimicrobial resistance (AMR)
in zoonotic bacteria isolated from humans, animals and food in the European Union (EU).
For 2014, 28 MSs reported data on AMR in zoonotic bacteria to the European Food Safety Authority
(EFSA), and 21 MSs submitted data to the European Centre for Disease Prevention and Control
(ECDC). In addition, three other European countries provided information. The enhanced monitoring
of AMR in bacteria from food and food-producing animals set out in the Commission Implementing
Decision 2013/652/EU was successfully implemented in reporting MSs and non-MSs in the EU during
2014. In accordance with the legislation, the 2014 AMR data on food and food-producing animals
specifically targeted different poultry populations and meat derived thereof. EFSA and ECDC
performed the analyses of the data, the results of which are published in this EU Summary Report on
AMR. Data on resistance were reported regarding Salmonella and Campylobacter isolates from
humans, poultry and meat thereof, whereas data on indicator Escherichia coli isolates were related
only to poultry and meat derived thereof. Some MSs also reported data on the occurrence of
meticillin-resistant Staphylococcus aureus (MRSA) in animals and food; the antimicrobial susceptibility
of MRSA isolates was additionally reported by two countries.
The quantitative data on AMR in isolates from humans, poultry and meat thereof were assessed using
harmonised epidemiological cut-off values that define microbiological resistance, i.e. reduced
susceptibility to the antimicrobials tested, as well as using clinical breakpoints (CBPs), where
considered appropriate. The categorical (qualitative) data on AMR in isolates from humans interpreted
by using CBPs were aligned with microbiological resistance by combining clinically resistant and
intermediate resistant isolates into a non-susceptible group. Isolates from different sources should
only be directly compared when methods and interpretive criteria are comparable.
For the first time, all MSs reported AMR data on poultry and meat thereof at the isolate level. This
enabled analysis of multi-drug resistance (MDR) and co-resistance patterns to critically important
antimicrobials in both human and animal isolates at the EU level but also at country level. In addition,
for all bacterial species, AMR data could be analysed at the production-type level, such as broilers and
laying hens of Gallus gallus and fattening turkeys, which allows the analysis of the data to be fine-
tuned. More specifically, reporting data at isolate level allowed characterisation of important patterns
of resistance, enabling Salmonella serovars to be linked to particular resistance patterns and to
identify high-level resistance to fluoroquinolones and important resistance phenotypes in both
Salmonella and indicator E. coli. The information published in this report provides an overview of
resistance in most MSs with detailed consideration of certain important aspects.
Highlights of this report include the continued monitoring of the spread of certain highly resistant
Salmonella serovars. Two serovars in particular, S. Infantis and S. Kentucky, contribute significantly to
the overall numbers of multidrug-resistant Salmonella in Europe. Both serovars display high-level
resistance to ciprofloxacin, which is an important public health concern because ciprofloxacin is a
common first-line treatment for invasive salmonellosis in humans.
The introduction of Commission implementing Decision 2013/652/EU with revised panels of
antimicrobials to be tested has been timely, preceding recent reports of emergence of transferable
colistin and erythromycin resistance in Asia (Liu et al., 2015; Wang et al., 2015). The continually
evolving threat from emerging resistance underlines the need to review the data collected, interpret
the findings and assess trends. This report has attempted to highlight some of the most important
findings in 2014, but space constraints mean that it is necessarily selective.
The inclusion within the harmonised monitoring scheme of a supplementary panel of antimicrobials, to
be tested when certain resistances to an initial panel of antimicrobials are detected, enabled detailed
screening of resistance to three carbapenem compounds. No resistance to meropenem was detected
and this is a crucial finding, because carbapenems are critically important in human medicine. Only
nine E. coli isolates from broilers and one from fattening turkeys isolated in 6 MSs showed resistance
to ertapenem, and all these isolates presented a putative extended spectrum beta-lactamase (ESBL)
or AmpC phenotype. These isolates are being further investigated.
The supplementary testing also allowed, for the first time, detailed characterisation of the beta-lactam
resistance phenotypes occurring in Salmonella and indicator E. coli. It enabled further phenotypic
characterisation of third-generation cephalosporin and carbapenem resistance in Salmonella and
indicator E. coli, by inferring presumptive profiles of ESBL-/AmpC-/carbapenemase-producers. The
occurrence of ESBL-/AmpC-producers in Salmonella and indicator E. coli from poultry was assessed as
being at low levels. It also showed that S. Infantis in Italy and S. Heidelberg in the Netherlands have
probably each acquired a different mechanism of third-generation cephalosporin resistance (an ESBL
enzyme in S. Infantis and an AmpC enzyme in S. Heidelberg) and have subsequently spread within
each MS.
isolates were recovered from a given animal/food category in a country to account for the low
prevalence of certain serovars and for the sake of completeness.
In humans
In 2014, 21 MSs and Norway reported data on AMR in Salmonella isolates from human cases of
salmonellosis. Twelve countries provided data as measured values (quantitative data), five more than
the previous year when this type of data collection was implemented. The reported data from the 22
countries represented 16.0% of the confirmed salmonellosis cases reported in the EU/European
Economic Area (EEA) in 2014.
High proportions of human Salmonella isolates were resistant to tetracyclines (30.3%), sulfonamides
(28.6%) and ampicillin (28.2%). MDR was high overall (26.0%) in the EU, with very high prevalence
in some countries. Some of the investigated serovars exhibited very high to extremely high MDR, such
as S. Kentucky (74.6%), monophasic S. Typhimurium 1,4,[5],12:i:- (69.4%) and S. Infantis (61.9%).
However, more than half (54.8%) of all isolates from humans were susceptible to the complete range
of antimicrobial classes tested. The proportions of Salmonella isolates resistant to the clinically
important antimicrobials ciprofloxacin and cefotaxime was overall relatively low (8.8% resistant to
ciprofloxacin and 1.1% to cefotaxime). The higher ciprofloxacin resistance in 2014 compared to 2013
is most likely due to a combination of the lowered European Committee on Antimicrobial Susceptibility
Testing (EUCAST, www.eucast.org) CBP for ciprofloxacin in 2014 now directly comparable with the
ECOFF and the implementation by a few countries of a better marker (pefloxacin) than ciprofloxacin
for screening with disk diffusion of low-level fluoroquinolone resistance in Salmonella.
An extremely high proportion (84.0%) of S. Kentucky was resistant to ciprofloxacin, which is
consistent with the dissemination of the ciprofloxacin-resistant S. Kentucky ST198 strain in Europe and
elsewhere since 2010 (Le Hello et al., 2013). Resistance to third-generation cephalosporins was more
common in S. Infantis and S. Kentucky with particularly high levels observed in Italy, most likely due
to the circulation of a multiresistant and ESBL-producing (cefotaximase (CTX-M) type) clone of
S. Infantis.
Clinical and microbiological co-resistance to ciprofloxacin and cefotaxime was overall very low in
Salmonella spp. (0.5% and 0.6%, respectively).
Resistance to colistin was commonly detected in S. Enteritidis (67.5%, two MSs) which could be due
to intrinsic resistance in this serovar (see text box Resistance to colistin). As the CBP is at the same
concentration as the ECOFF applied in the analysis, the observed colistin resistance is of concern since
this last-resort drug might no longer be effective for treating severe human infections with the most
common Salmonella serovar.
Generally, low to very low levels of microbiological co-resistance to ciprofloxacin and cefotaxime in
Salmonella spp. from broiler flocks (1.8%) and laying hen flocks (0.12%) were reported. When the
resistance to ciprofloxacin and cefotaxime was interpreted using CBPs, only one S. Kentucky isolate
from broilers in Spain displayed clinical resistance.
Among all serovars, isolates resistant to ciprofloxacin, but not to nalidixic acid, were observed,
probably indicating an increasing occurrence of plasmid-mediated quinolone resistance.
Among Salmonella spp. isolates from poultry populations, most MSs reported moderate or high to
extremely high resistance to tetracyclines and sulfonamides, and similar or slightly lower levels of
ampicillin resistance. Resistance levels were generally higher in isolates from fattening turkeys than
from broilers and laying hens.
Overall, high levels of resistance to ciprofloxacin and nalidixic acid were observed in Salmonella spp.
isolates from fattening turkeys and broilers compared with the moderate levels recorded in
Salmonella spp. isolates from laying hens. Resistance to third-generation cephalosporins (cefotaxime
and ceftazidime) was generally at very low or low levels in Salmonella spp. isolates from broilers and
laying hens in most reporting MSs, with the striking exception of the high levels of cefotaxime and
ceftazidime resistance reported in Salmonella spp. from broilers in Italy. No resistance to third-
generation cephalosporins was detected in fattening turkeys.
Clinical resistance to cefotaxime was found at low to high levels in Salmonella spp. isolates from
broilers and laying hens in 10 MSs. The supplementary testing performed in 2014 allowed further
phenotypic characterisation of those Salmonella isolates which were resistant to third-generation
cephalosporins.
Most Salmonella spp. isolates from broilers with an ESBL phenotype were S. Infantis (18/30, 60%)
with S. Paratyphi B L(+) tartrate positive (S. Paratyphi B var. Java) comprising a further 6/30 (20%).
Considering those isolates with an AmpC phenotype, 9/18 (50%) were S. Heidelberg, whereas single
isolates of S. Infantis and S. Paratyphi B var. Java had an AmpC phenotype. Salmonella spp. from
broilers with an AmpC and an ESBL phenotype included three isolates of S. Infantis and a single
isolate of S. Enteritidis. Three Salmonella isolates from laying hens with an AmpC phenotype belonged
to serovars S. Enteritidis, S. Anatum and S. Glostrup.
Resistance to carbapenems in Salmonella in poultry and meat thereof was not observed in any of the
reporting countries.
Broilers and fattening turkeys were the main focus of the monitoring in 2014 in accordance with
Decision 2013/652/EU. The detailed reporting of results at serovar level clearly demonstrates the
major contribution of a few serovars to the observed prevalence of resistance in Salmonella. In
broilers, eight serovars (Infantis, Enteritidis, Mbandaka, Kentucky, Senftenberg, Typhimurium, Agona
and Montevideo) accounted for 74.1% of Salmonella spp. (Figure 1) and in laying hens eight serovars
(Enteritidis, Typhimurium, Infantis, Kentucky, Montevideo, Mbandaka, Senftenberg and Livingstone)
accounted for 62.3% of Salmonella spp. In fattening turkeys, eight serovars (Derby, Kentucky,
Newport, Hadar, Infantis, Saintpaul, Bredeney and Stanley) accounted for 68.1% of Salmonella spp.
Patterns of resistance associated with these serovars, may therefore be expected to have a marked
influence on the overall resistance levels in Salmonella from these types of poultry (Figure 2).
S. Senftenberg, 4.5
S. Infantis*
S. Kentucky, 4.8
Salmonella other serovars
S. Enteritidis
S. Mbandaka, 6.8
S. Infantis, 36.6 S. Mbandaka
S. Kentucky
S. Senftenberg
S. Enteritidis, 13.5
S. Typhimurium
Salmonella other S. Agona
serovars, 25.9
S. Montevideo
Figure 1: Breakdown of serovars in Salmonella isolates from broiler flocks tested for antimicrobial
susceptibility in the EU, 2014
S. Infantis (N=797)
Resistant to one
monophasic S.Typhimurium (N=31) or two
antimicrobials
S.Typhimurium (N=83)
Multi-resistant
S. Enteriditis (N=304)
0 20 40 60 80 100
Figure 2: Proportions of isolates fully susceptible, resistant to one to two classes of substances and
multiresistant in the most commonly recovered Salmonella serovars in broiler flocks in
the EU, 2014
S. Infantis is a dominant serovar in broilers, accounting for 35.9% of all Salmonella isolates examined
from broilers (762/2,122), and commonly showing resistance. The proportion of all isolates showing
MDR in broilers was also greatly influenced by the occurrence of multiresistant S. Infantis, this serovar
accounting for approximately 31% of the multiresistant isolates in broilers. Particular MDR patterns
were associated with S. Infantis and because this serovar was prevalent in many countries, these
patterns greatly influenced the overall resistance figures. Underlining the significance of resistance in
S. Infantis, resistance to third-generation cephalosporins in isolates from broilers in Italy (with a
presumptive ESBL phenotype) and high-level resistance to ciprofloxacin were both detected in this
serovar. High-level ciprofloxacin resistance was otherwise detected mainly in S. Kentucky, a further
significant serovar in poultry in Europe in 2014.
In contrast, S. Enteritidis was less commonly multiresistant than S. Infantis, although one isolate was
identified with an ESBL and AmpC phenotype. Higher levels of resistance to colistin were observed for
S. Enteritidis than for other Salmonella serovars. This has been reported previously (Agers et al.,
2012) and is considered to reflect probable intrinsic differences in susceptibility for certain serovars of
Salmonella (so-called group D Salmonella according to the Kauffman-White Scheme, Grimont and
Weill, 2013).
High-level resistance to ciprofloxacin was most often observed in S. Kentucky isolates from
Gallus gallus in Cyprus, Hungary, Italy, Romania and Spain, and from turkeys in the Czech Republic,
Hungary, Italy, Poland and Spain and in broiler meat from Hungary and Spain. Most of the
S. Kentucky isolates with high-level ciprofloxacin resistance (n=161) were multiresistant (73.3%).
S. Kentucky with high-level ciprofloxacin resistance is likely to belong to the multilocus sequence type
ST198 clone, which has shown epidemic spread in North Africa and the Middle East (Le Hello, 2013a).
Colistin-resistant Salmonella isolates were found by several MSs originating from broilers, laying hens
and fattening turkeys. Further information is provided in the text box below.
Microbiological resistance to tigecycline was reported in 9.3% of all Salmonella spp. from broilers,
0.6% of isolates from laying hens and 8% from turkeys. There was a marked association of
tigecycline microbiological resistance with S. Infantis in poultry and most microbiologically resistant
strains had minimum inhibitory concentrations (MICs) just above the ECOFF at 2 or 4 mg/l. Resistance
to tigecycline in Salmonella is thought to be mediated by increased activity of efflux pumps, through
modifications to the expression of efflux pump regulatory genes and this may explain the distribution
of MICs which was obtained. Determining the susceptibility of tigecycline is not entirely
straightforward as the method can be affected by oxidation of the reagents and the tigecycline results
are being further investigated by the European Union Reference Laboratory for AMR (EURL-AR,
www.crl-ar.eu).
In humans
In 2014, 13 MSs and Norway reported data on AMR in Campylobacter isolates from human cases of
campylobacteriosis. Eight countries provided data as measured values (quantitative data), three more
than the previous year when this type of data collection was implemented. The reported data from
the 14 countries represented 12.3% and 17.4% of the confirmed human cases with Campylobacter
jejuni and Campylobacter coli, respectively, reported in the EU/EEA in 2014.
The proportion of human C. jejuni isolates resistant to erythromycin was overall low, but moderately
high in C. coli and high (> 20.050.0%) to very high (> 50.070.0%) in C. coli in a few reporting
countries. Very high to extremely high resistance levels to ciprofloxacin were reported in human
Campylobacter isolates from all reporting MSs (although lower in Norway). Five of 13 MSs reported
ciprofloxacin resistance in > 80% of isolates and one country in 97.7%; in such settings, effective
treatment options for human enteric Campylobacter infection are significantly reduced. Given the high
levels of resistance to fluoroquinolones in broilers and the assessment that a large proportion of
human campylobacteriosis infections comes from handling, preparation and consumption of broiler
meat (EFSA BIOHAZ Panel, 2010a), this is a compelling example of how AMR in food and animals may
impact the availability of effective antimicrobial agents for treating severe human Campylobacter
infections. High levels of tetracycline resistance were also observed (46.4% for C. jejuni and 53.8%
for C. coli).
Co-resistance to the critically important antimicrobials ciprofloxacin and erythromycin varied by
country but was overall low (0.3%) in C. jejuni and moderate in C. coli (13.6%). In the case of C. coli,
two MSs reported co-resistance in 44.857.6% of isolates. Multidrug resistance, i.e. microbiological
resistance to at least three of the four different antimicrobial classes, was low (0.4%) in C. jejuni but
markedly higher (13.6%) in C. coli.
was respectively low (5.9%) and very low (0.9%). A similar pattern of resistance to these substances
occurred in C. coli from broilers, although at overall higher levels than those observed in C. jejuni, at
74.3%, 69.5% and 59.6%, for ciprofloxacin, nalidixic acid and tetracycline and at 14.5% and 2.6% for
erythromycin and gentamicin, respectively.
Multidrug resistance (reduced susceptibility to at least three antimicrobial classes according to
ECOFFs) was overall low (4.6%) in C. jejuni from broilers. Co-resistance to the criticially important
antimicrobials ciprofloxacin and erythromycin was either not detected or recorded up to high levels
(overall, at 4.8%). The situation was different for C. coli from broilers, where MDR as a percentage of
all isolates received by the individual MSs ranged from 2.8% to 33.3% (overall MDR at 13.6%) in the
reporting MSs.
Over the 20082014 period, resistance to ciprofloxacin, erythromycin and nalidixic acid in broilers
varied greatly among reporting MSs and statistically significant increasing trends in resistance to these
antimicrobials were observed for several MSs, for both C. jejuni and C. coli.
In C. jejuni isolates from broiler meat, resistance, considering all reporting MSs, ranged from high to
very high for ciprofloxacin (65.7%), nalidixic acid (61.8%) and tetracyclines (36.3%), whereaslevels of
resistance to erythromycin and gentamicin were low at 1.6% and very low 0.3%, respectively. A
similar pattern was observed for C. coli isolates from broiler meat; however, levels of resistance were
higher overall. Levels of resistance to ciprofloxacin and nalidixic acid were extremely high at 85.8%
and 85.1%, respectively, very high for tetracycline at 73.9%, moderate for erythromycin at 17.2%
and not detected for gentamicin.
Despite the fact that imported food can contribute to cases of Campylobacter infection, there were
striking parallels in the observed occurrence of resistance to ciprofloxacin, erythromycin, gentamicin
and tetracyclines in C. jejuni isolates from broiler meat, broilers and humans in Austria and in C. coli
isolates from broiler meat and humans in Portugal, with similar levels of resistance to each
antimicrobial seen in isolates originating from these different sources within each country. Austria and
Portugal were the only MSs who reported results for Campylobacter isolates from meat and from
human cases of infection. Interestingly, Austria also reported results for C. jejuni from meat from
turkeys and fattening turkeys; isolates from turkeys also closely paralleled the results obtained for
isolates from human cases, whereas ciprofloxacin resistance was rather higher in isolates from turkey
meat.
MDR levels (reduced susceptibility to at least three antimicrobial classes according to ECOFFs) were
generally very high in indicator E. coli isolates from broilers (overall 54.6%), with extremely high level
in a number of reporting countries. Co-resistance/reduced susceptibility to the clinically important
antimicrobials, ciprofloxacin and cefotaxime, was also detected in 4.0% of isolates from broilers.
When the resistance to ciprofloxacin and cefotaxime was interpreted using CBPs, only 1.9% isolates
from broilers displayed clinical resistance.
In the reporting group of MSs, resistance levels in indicator E. coli isolates from fattening turkeys were
generally lower than among isolates from broilers. The highest resistance levels observed were to
tetracyclines (70.9%), ampicillin (69.0%), sulfamethoxazole (51.1%), ciprofloxacin (50.3%) and
nalidixic acid (43.5%). The occurrence of resistance was variable between MSs for most of the
antimicrobials. Overall, only a few isolates (2.3%) expressed resistance to cefotaxime and 2.2% to
ceftazidime.
MDR (reduced susceptibility to at least three of the eleven antimicrobial classes tested) was overall
very high in fattening turkeys (59.3%). Generally low levels of microbiological co-resistance to
ciprofloxacin and cefotaxime in E. coli from fattening turkeys were reported and when the resistance
to ciprofloxacin and cefotaxime was interpreted using clinical breakpoints, only few isolates displayed
clinical resistance (overall at 0.8%).
Strains of E. coli are not separated on phenotypic characteristics (e.g. serotype) in the current
monitoring programme and a less detailed analysis is therefore possible than for Salmonella where
isolates can be sub-divided by serovar. A common core of microbiological resistance to ampicillin,
ciprofloxacin/nalidixic acid, sulfamethoxazole, tetracycline and trimethoprim was observed in 41.2% of
all E .coli isolates from broilers. In fattening turkeys, one MDR pattern was predominant (ampicillin,
chloramphenicol, ciprofloxacin/nalidixic acid, tetracycline, sulfamethoxazole and trimethoprim) and
accounted for more than 20.0% of the MDR patterns in E. coli isolates from fattening turkeys and
12.5% E. coli isolates data available. In contrast to the situation in Salmonella, tigecycline resistance
was infrequently detected in E. coli.
Colistin-resistant indicator E. coli isolates were found by several MSs originating from broilers and
fattening turkeys. Further information is provided in the text box below.
Monitoring was enhanced in 2014 to allow further characterisation of third-generation cephalosporin
and carbapenem resistance in indicator E. coli. The presumptive ESBL phenotype alone was more
frequently detected than the AmpC phenotype in indicator E. coli from both broiler and fattening
turkeys, although at low levels, in less than 5% of isolates in each animal population. An AmpC
together with an ESBL phenotype was detected in 0.5% of isolates from broilers, but was not
detected in isolates from fattening turkeys. Indicator E. coli is considered to represent a reservoir of
ESBL and AmpC resistance, which may be transferred to other organisms such as Salmonella. The
proportions of indicator E. coli showing such ESBL and AmpC phenotypic resistance were higher than
those observed in Salmonella (Table 2: below), but more detailed investigations, including comparison
of resistance genes and plasmids, would be required to confirm the inferred phenotype and
investigate whether there was any direct relationship between the resistance detected in the
populations of E. coli and Salmonella included in the monitoring.
The MIC distributions reveal the presence of Salmonella and E. coli isolates with colistin MICs
> 2 mg/L; however, as mentioned above, it has been previously recognised that certain Salmonella
serovars belonging to group D in the KauffmannWhite typing scheme (which possess O:9 somatic
antigens) are intrinsically resistant to colistin at higher levels than other non-Group D serovars (Agers
et al., 2012). Group D Salmonella serovars include S. Enteritidis which is highly represented among
the Salmonella isolates tested in broilers, accounting for 13.5% of isolates. Colistin resistance was
observed in 8.3% of all Salmonella isolates from broilers and 10.5% from laying hens; 72% of these
colistin-resistant Salmonella isolates from broilers and 80% from laying hens were S. Enteritidis. A
large proportion of the resistance to colistin detected in Salmonella in Gallus gallus therefore appears
to be related to the previously described higher level of intrinsic resistance of S. Enteritidis. According
to some of the reports mentioned above, for other serovars such as S. Paratyphi B var. Java,
S. Schwarzengrund, S. Typhimurium and or monofasic variants, the presence of mcr-1 could play a
role.
For the first time in 2014, colistin resistance was monitored in indicator E. coli in poultry, and 0.9% of
E. coli from broilers and 7.4% of E. coli from turkeys were resistant to colistin in the reporting MSs.
reported. The increase is primarily the result of the diffusion within the Swiss population of fattening
pigs of clones of spa-types t034 and t011, both belonging to the clonal complex CC398.
Monitoring for MRSA in food and animals is performed on a voluntary basis and consequently a
relatively low number of MSs/non-MSs (four) reported the results of MRSA monitoring of either food
and/or food-producing animals. MRSA detection methods can be very susceptible and consequently
detect low levels of the organism; food is not currently regarded as a source of livestock-associated
MRSA infection for humans. Three isolates of a healthcare-associated MRSA (spa-type t032) recovered
from broiler meat at retail may have originated from human sources, as this spa-type is not well-
recognised in animals, but is common in humans in some countries.
The voluntary monitoring performed reflects the priorities of MSs and although monitoring is not co-
ordinated across MSs, LA-MRSA is evidently widespread geographically and in diverse mammalian and
avian host species. It is unclear whether the broad range of species in which colonisation has been
detected reflects diffusion in those different species and long-term colonisation, or transient cross-
colonisation between species on mixed farms, from species in which colonisation occurs readily, such
as pigs.
Table of contents
Abstract .........................................................................................................................................1
Summary .......................................................................................................................................3
List of tables ................................................................................................................................ 16
List of figures ............................................................................................................................... 18
Legal basis ................................................................................................................................... 21
1. Introduction...................................................................................................................... 22
1.1. Monitoring and reporting of antimicrobial resistance at the EU level ..................................... 22
1.2. Further harmonised monitoring of antimicrobial resistance .................................................. 22
1.2.1. New legislation on antimicrobial resistance monitoring in animals and food .......................... 23
1.2.2. Developments in the harmonised monitoring of antimicrobial resistance in humans .............. 23
1.3. The 2014 EU Summary Report on AMR .............................................................................. 24
2. Materials and methods ...................................................................................................... 25
2.1. Antimicrobial susceptibility data from humans available in 2014 ........................................... 25
2.1.1. Salmonella data of human origin ........................................................................................ 25
2.1.2. Campylobacter data of human origin .................................................................................. 26
2.2. Antimicrobial susceptibility data from animals and food in 2014 ........................................... 29
2.2.1. Data reported under Directive 2003/99/EC and Decision 2013/652/EU ................................. 29
2.2.2. Data validation.................................................................................................................. 33
2.2.3. Analyses of antimicrobial resistance data ............................................................................ 33
2.2.4. Analysis of multidrug resistance and co-resistance data ....................................................... 35
2.2.5. Identification of presumptive phenotypes of ESBL-, AmpC- and/or
carbapenemase-producers ................................................................................................. 36
2.2.6. Data on meticillin-resistant Staphylococcus aureus (MRSA) .................................................. 37
3. Assessment ...................................................................................................................... 38
3.1. Antimicrobial resistance in Salmonella ................................................................................ 38
3.1.1. Antimicrobial resistance in Salmonella isolates from humans ................................................ 38
3.1.2. Antimicrobial resistance in Salmonella isolates from animals and food .................................. 60
3.1.3. Discussion ...................................................................................................................... 106
3.2. Antimicrobial resistance in Campylobacter ........................................................................ 110
3.2.1. Antimicrobial resistance in Campylobacter isolates from humans ........................................ 110
3.2.2. Antimicrobial resistance in Campylobacter isolates from animals and food .......................... 115
3.2.3. Discussion ...................................................................................................................... 127
3.3. Antimicrobial resistance in indicator Escherichia coli .......................................................... 132
3.3.1. Antimicrobial resistance in indicator Escherichia coli isolates from animals .......................... 133
3.3.2. Multiple drug resistance patterns in indicator Escherichia coli isolates ................................. 149
3.3.3. Discussion ...................................................................................................................... 151
3.4. Meticillin-resistant Staphylococcus aureus ......................................................................... 154
3.4.1. Meticillin-resistant Staphylococcus aureus in food and animals ........................................... 154
3.4.2. Discussion ...................................................................................................................... 160
3.5. Third-generation cephalosporin and carbapenem resistance in Escherichia coli and
Salmonella ...................................................................................................................... 163
3.5.1. Third-generation cephalosporin and carbapenem resistance in Salmonella isolates from food
and animals (routine monitoring) ..................................................................................... 165
3.5.2. Third-generation cephalosporin and carbapenem resistance in indicator Escherichia coli
isolates from food and animals (routine monitoring) .......................................................... 168
3.5.3. Specific monitoring of ESBL-/AmpC-/carbapenemase-producing E. coli ............................... 173
3.5.4. Comparison of cefotaxime resistance in Salmonella spp. and indicator Escherichia coli
isolates from animals....................................................................................................... 179
3.5.5. Discussion ...................................................................................................................... 181
References ................................................................................................................................. 184
List of abbreviations ................................................................................................................... 190
Appendix: List of usable data ...................................................................................................... 194
List of tables
Table 30: Resistance in indicator E. coli from broilers assessed by the percentage of resistant
isolates (Total) and summary indicator (weighted mean of the proportions of resistant
isolates in the reporting MSs) in the EU, 27 MSs, 2014 ................................................ 145
Table 31: Occurrence of resistance to selected antimicrobials in indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014 ......................................................... 146
Table 32: Co-resistance to fluoroquinolones and third-generation cephalosporins in indicator
Escherichia coli from fattening turkeys in MSs, 2014 ................................................... 149
Table 33: Meticillin-resistant Staphylococcus aureus in food, 2014 .............................................. 155
Table 34: Meticillin-resistant Staphylococcus aureus in food-producing animals (excluding clinical
investigations), 2014................................................................................................. 156
Table 35: Meticillin-resistant Staphylococcus aureus in food-producing animals, clinical
investigations, 2014 .................................................................................................. 157
Table 36: Meticillin-resistant Staphylococcus aureus in companion animals, clinical investigations,
2014 ........................................................................................................................ 158
Table 37: Temporal occurrence of meticillin-resistant Staphylococcus aureus in animals .............. 159
Table 38: Occurrence of resistance (%) to selected antimicrobials in MRSA from food and animals,
2014 ........................................................................................................................ 160
Table 39: Occurrence of resistance to beta-lactam compounds in Salmonella spp. isolates from
broilers, laying hens and meat from broilers collected within the routine monitoring and
subjected to supplementary testing (panel 2) in 2014 ................................................. 166
Table 40: Presumptive ESBL and AmpC phenotypes identified in Salmonella spp. isolates from
broilers, laying hens and meat from broilers collected within the routine monitoring and
subjected to supplementary testing (panel 2) in 2014(a) .............................................. 167
Table 41: Occurrence of resistance to beta-lactam and carbapenem compounds in indicator E. coli
isolates from broiler flocks collected within the routine monitoring and subjected to
supplementary testing (panel 2) in 2014 .................................................................... 169
Table 42: Presumptive ESBL and AmpC phenotypes identified in indicator E. coli isolates from broiler
flocks collected within the routine monitoring and subjected to supplementary testing
(panel 2) in 2014 ...................................................................................................... 170
Table 43: Occurrence of resistance to beta-lactam and carbapenem compounds in indicator E. coli
isolates from fattening turkeys collected within the routine monitoring and subjected to
supplementary testing (panel 2) in 2014 .................................................................... 171
Table 44: Presumptive ESBL and AmpC phenotypes identified in indicator E. coli isolates from
fattening turkeys collected within the routine monitoring and subjected to supplementary
testing (panel 2) in 2014 .......................................................................................... 172
Table 45: Prevalence of carbapenemase-producing E. coli from broilers and fattening turkeys
collected within the specific carbapenemase-producing microorganisms monitoring in Italy
in 2014 .................................................................................................................... 174
Table 46: Prevalence of ESBL-/AmpC-producing E. coli from broilers and fattening turkeys within
the specific ESBL-/AmpC-producing E. coli monitoring in Italy in 2014 ......................... 174
Table 47: Prevalence of ESBL-/AmpC-producing Salmonella from broilers and fattening turkeys
within national specific ESBL-/AmpC-producing Salmonella monitoring in Italy in 2014 .. 175
Table 48: Occurrence of resistance to selected antimicrobials in Escherichia coli from broilers and
fattening turkeys in reporting countries collected within thespecific ESBL-/Ampc-
/carbapenemase-producing monitoring (Panel 1), in 2014 ........................................... 176
Table 49: Occurrence of resistance to selected antimicrobials in Escherichia coli from broilers and
fattening turkeys in reporting countries collected within the specific ESBL-/Ampc-
/carbapenemase-producing monitoring (Panel 1), in 2014 ........................................... 177
Table 50: Presumptive ESBL and AmpC phenotypes identified in E. coli isolates from meat from
broilers, broilers and fattening turkeys collected within the specific ESBL-/Ampc-
/carbapenemase-producing monitoring and subjected to supplementary testing or
molecular typing confirmation in 2014(a) ..................................................................... 178
Table 51: Resistance (%) to cefotaxime and ceftazidime in Salmonella spp. and indicator E. coli
isolates in MSs in 2014 testing both bacterial species in broilers or fattening turkeys .... 180
List of figures
Figure 1: Breakdown of serovars in Salmonella isolates from broiler flocks tested for antimicrobial
susceptibility in the EU, 2014 .......................................................................................7
Figure 2: Proportions of isolates fully susceptible, resistant to one to two classes of substances and
multiresistant in the most commonly recovered Salmonella serovars in broiler flocks in
the EU, 2014 ...............................................................................................................7
Figure 3: Erythromycin resistance in C. jejuni and C. coli from broilers ........................................ 10
Figure 4: Erythromycin resistance in C. jejuni and C. coli from fattening turkeys .......................... 10
Figure 5: Colistin resistance in Salmonella ................................................................................. 12
Figure 6: Colistin resistance in indicator E. coli........................................................................... 13
Figure 7: Comparison of CBPs for non-susceptibility (intermediate and resistant categories
combined) and ECOFFs used to interpret MIC data reported for Salmonella spp. from
humans, animals or food ............................................................................................ 39
Figure 8: Frequency distribution of Salmonella spp. isolates from humans completely susceptible or
resistant to one to eight antimicrobial classes in 2014 .................................................. 41
Figure 9: Frequency distribution of Salmonella Enteritidis isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014 ............................. 44
Figure 10: Spatial distribution of ciprofloxacin resistance among S. Enteritidis from human cases in
reporting countries in 2014 ........................................................................................ 47
Figure 11: Spatial distribution of nalidixic acid resistance among S. Enteritidis from human cases in
reporting countries in 2014 ........................................................................................ 48
Figure 12: Spatial distribution of cefotaxime resistance among S. Enteritidis from human cases in
reporting countries in 2014 ........................................................................................ 48
Figure 13: Frequency distribution of Salmonella Infantis isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014 ............................. 49
Figure 14: Spatial distribution of ciprofloxacin resistance among S. Infantis from human cases in
reporting countries in 2014 ........................................................................................ 52
Figure 15: Spatial distribution of nalidixic acid resistance among S. Infantis from human cases in
reporting countries in 2014 ........................................................................................ 53
Figure 16: Spatial distribution of cefotaxime resistance among S. Infantis from human cases in
reporting countries in 2014 ........................................................................................ 53
Figure 17: Frequency distribution of Salmonella Kentucky isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014 ............................. 54
Figure 18: Frequency distribution of Salmonella Typhimurium isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014 ............................. 59
Figure 19: Frequency distribution of monophasic Salmonella Typhimurium 1,4,[5],12:i:- isolates
from humans completely susceptible or resistant to one to eight antimicrobial classes in
2014 ......................................................................................................................... 60
Figure 20: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobial classes in Salmonella spp. from broiler meat in MSs in 2014 .............. 61
Figure 21: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobial classes in Salmonella spp. from fattening turkey meat in MSs in 2014 62
Figure 22: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from broilers in MSs in 2014 ................... 64
Figure 23: Spatial distribution of ciprofloxacin resistance among Salmonella spp. from broilers in
countries reporting MIC data in 2014 .......................................................................... 65
Figure 24: Spatial distribution of nalidixic acid resistance among Salmonella spp. from broilers in
countries reporting MIC data in 2014 .......................................................................... 66
Figure 25: Spatial distribution of cefotaxime resistance among Salmonella spp. from broilers in
countries reporting MIC data in 2014 .......................................................................... 66
Figure 26: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Infantis from broilers in MSs in 2014 .............. 69
Figure 27: Spatial distribution of ciprofloxacin resistance among Salmonella Infantis from broilers in
countries reporting MIC data in 2014 .......................................................................... 70
Figure 28: Spatial distribution of nalidixic acid resistance among Salmonella Infantis from broilers in
countries reporting MIC data in 2014 .......................................................................... 70
Figure 29: Spatial distribution of cefotaxime resistance among Salmonella Infantis from broilers in
countries reporting MIC data in 2014 .......................................................................... 71
Figure 30: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Enteritidis from broilers in MSs in 2014 ........... 72
Figure 31: Spatial distribution of ciprofloxacin resistance among Salmonella Enteritidis from broilers
in countries reporting MIC data in 2014 ...................................................................... 73
Figure 32: Spatial distribution of nalidixic acid resistance among Salmonella Enteritidis from broilers
in countries reporting MIC data in 2014 ...................................................................... 73
Figure 33: Spatial distribution of cefotaxime resistance among Salmonella Enteritidis from broilers in
countries reporting MIC data in 2014 .......................................................................... 74
Figure 34: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Kentuky from broilers in MSs in 2014 ............. 75
Figure 35: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from laying hens in MSs in 2014 ............. 80
Figure 36: Spatial distribution of ciprofloxacin resistance among Salmonella spp. from laying hens in
countries reporting MIC data in 2014 .......................................................................... 81
Figure 37: Spatial distribution of nalidixic acid resistance among Salmonella spp. from laying hens in
countries reporting MIC data in 2014 .......................................................................... 81
Figure 38: Spatial distribution of cefotaxime resistance among Salmonella spp. from laying hens in
countries reporting MIC data in 2014 .......................................................................... 82
Figure 39: Trends in ampicillin, cefotaxime, ciprofloxacin and nalidixic acid resistance in tested
Salmonella spp. isolates from Gallus gallus in reporting MSs, 20082014, quantitative
data.......................................................................................................................... 83
Figure 40: Trends in ampicillin, cefotaxime, ciprofloxacin and nalidixic acid resistance in tested
Salmonella Enteritidis isolates from Gallus gallus in reporting MSs, 20082014,
quantitative data ....................................................................................................... 84
Figure 41: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Enteritidis from laying hens in MSs in 2014 ..... 87
Figure 42: Spatial distribution of ciprofloxacin resistance among Salmonella Enteritidis from laying
hens in countries reporting MIC data in 2014 .............................................................. 88
Figure 43: Spatial distribution of nalidixic acid resistance among Salmonella Enteritidis from laying
hens in countries reporting MIC data in 2014 .............................................................. 88
Figure 44: Spatial distribution of cefotaxime resistance among Salmonella Enteritidis from laying
hens in countries reporting MIC data in 2014 .............................................................. 89
Figure 45: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Infantis from laying hens in MSs in 2014 ........ 90
Figure 46: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Kentucky from laying hens in MSs in 2014 ...... 90
Figure 47: Trends in ampicillin, cefotaxime, ciprofloxacin and nalidixic acid resistance in tested
Salmonella spp. isolates from turkeys in reporting MSs, 20082014, quantitative data ... 98
Figure 48: Spatial distribution of ciprofloxacin resistance among Salmonella spp. from fattening
turkeys in 2014 ......................................................................................................... 99
Figure 49: Spatial distribution of nalidixic acid resistance among Salmonella spp. from fattening
turkeys in 2014 ......................................................................................................... 99
Figure 50: Spatial distribution of cefotaxime resistance among Salmonella spp. from fattening
turkeys in 2014 ....................................................................................................... 100
Figure 51: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from fattening turkeys in 2014 .............. 100
Figure 52: Tigecycline resistance in Salmonella spp. .................................................................. 109
Figure 53: Comparison of CBPs and ECOFFs used to interpret MIC data reported for
Campylobacter spp. from humans, animals or food.................................................... 111
Figure 54: Frequency distribution of Campylobacter jejuni isolates from humans completely
susceptible or resistant to one to four antimicrobial classes in 2014 ............................ 112
Figure 55: Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from human
cases in reporting countries in 2014 ......................................................................... 113
Figure 56: Spatial distribution of erythromycin resistance among Campylobacter jejuni from human
cases in reporting countries in 2014 ......................................................................... 113
Figure 57: Frequency distribution of Campylobacter coli isolates from humans completely susceptible
or resistant to one to four antimicrobial classes in 2014 ............................................. 114
Figure 58: Trends in ciprofloxacin, erythromycin and nalidixic acid resistance in Campylobacter jejuni
from broilers in MSs, 20082014 .............................................................................. 119
Figure 59: Trends in ciprofloxacin, erythromycin and nalidixic acid resistance in Campylobacter coli
from broilers in MSs, 20082014 .............................................................................. 120
Figure 60: Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from broilers
of Gallus gallus in reporting countries in 2014 ........................................................... 121
Figure 61: Spatial distribution of erythromycin resistance among Campylobacter jejuni from broilers
of Gallus gallus in reporting countries in 2014 ........................................................... 121
Figure 62: Frequency distribution of Campylobacter jejuni isolates completely susceptible and
resistant to one to four antimicrobials, in broilers in MSs, 2014 .................................. 123
Figure 63: Frequency distribution of Campylobacter coli isolates completely susceptible and resistant
to one to four antimicrobials, in broilers in MSs, 2014 ................................................ 123
Figure 64: Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from fattening
turkeys in reporting countries in 2014 ....................................................................... 126
Figure 65: Spatial distribution of erythromycin resistance among Campylobacter jejuni from
fattening turkeys in reporting countries in 2014 ......................................................... 126
Figure 66: Frequency distribution of Campylobacter jejuni isolates completely susceptible and
resistant to one to four antimicrobials, in fattening turkeys in MSs, 2014 .................... 127
Figure 67: Erythromycin resistance in C. jejuni and C. coli from broilers and fattening turkeys ..... 131
Figure 68: Trends in ampicillin and tetracyclines resistance in indicator Escherichia coli from broilers
in reporting countries, 20082014 ............................................................................ 137
Figure 69: Trends in cefotaxime, ciprofloxacin and nalidixic acid resistance in indicator
Escherichia coli from broilers in reporting countries, 20082014 ................................. 138
Figure 70: Spatial distribution of ciprofloxacin resistance among indicator Escherichia coli from
broilers in reporting countries, in 2014 ...................................................................... 139
Figure 71: Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from
broilers in reporting countries, in 2014 ...................................................................... 139
Figure 72: Spatial distribution of cefotaxime resistance among indicator Escherichia coli from broilers
in reporting countries, in 2014.................................................................................. 140
Figure 73: Frequency distribution of Escherichia coli isolates completely susceptible and resistant to
one to twelve antimicrobials in broilers in reporting countries, 2014 ........................... 141
Figure 74: Spatial distribution of ciprofloxacin resistance among indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014 ........................................................ 147
Figure 75: Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014 ........................................................ 147
Figure 76: Spatial distribution of cefotaxime resistance among indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014 ........................................................ 148
Figure 77: Frequency distribution of Escherichia coli isolates completely susceptible and resistant to
one to 12 antimicrobials in fattening turkeys in MSs, 2014 ......................................... 148
Legal basis
According to Directive 2003/99/EC on the monitoring of zoonoses and zoonotic agents, Member States
(MSs) are obliged to monitor and report antimicrobial resistance (AMR) in Salmonella and
Campylobacter isolates obtained from healthy food-producing animals and from food. Commission
Implementing Decision 2013/652/EU of 12 November 2013 1 sets up priorities for the monitoring of
AMR from a public health perspective, establishes a list of combinations of bacterial species, food-
producing animal populations and foodstuffs and lays down detailed requirements on the harmonised
monitoring and reporting of AMR.
The data collection on human diseases from MSs is conducted in accordance with Decision
1082/2013/EU2 on serious cross-border threats to health, which in October 2013 replaced Decision
2119/98/EC on setting up a network for the epidemiological surveillance and control of communicable
diseases in the European Union (EU). The case definitions to be followed when reporting data on
infectious diseases, including AMR, to the European Centre for Disease Prevention and Control (ECDC)
are described in Decision 2012/506/EU3. ECDC has provided data on zoonotic infections in humans, as
well as their analyses, for the Community Summary Reports since 2005. Since 2007, data on human
cases have been reported from The European Surveillance System (TESSy), maintained by ECDC.
About EFSA
The European Food Safety Authority (EFSA), located in Parma, Italy, and established and funded by
the EU as an independent agency in 2002, provides objective scientific advice, in close collaboration
with national authorities and in open consultation with its stakeholders, with a direct or indirect impact
on food and feed safety, including animal health and welfare and plant protection. EFSA is also
consulted on nutrition in relation to EU legislation. EFSAs risk assessments provide risk managers (the
European Commission (EC), the European Parliament and the Council) with a sound scientific basis for
defining policy-driven legislative or regulatory measures required to ensure a high level of consumer
protection with regard to food and feed safety. EFSA communicates to the public in an open and
transparent way on all matters within its remit. Collection and analysis of scientific data, identification
of emerging risks and scientific support to the EC, particularly in the case of a food crisis, are also part
of EFSAs mandate, as laid down in founding Regulation (EC) No 178/20024 of 28 January 2002.
About ECDC
The European Centre for Disease Prevention and Control (ECDC), an EU agency based in Stockholm,
Sweden, was established in 2005. The objective of ECDC is to strengthen Europes defences against
infectious diseases. According to Article 3 of founding Regulation (EC) No 851/20045 of 21 April 2004,
ECDCs mission is to identify, assess and communicate current and emerging threats to human health
posed by infectious diseases. In order to achieve this goal, ECDC works in partnership with national
public health bodies across Europe to strengthen and develop EU-wide disease surveillance and early
warning systems. By working with experts throughout Europe, ECDC pools Europes knowledge in
health to develop authoritative scientific opinions about the risks posed by current and emerging
infectious diseases.
Terms of reference
The EU system for the monitoring and collection of information on zoonoses is based on the Zoonoses
Directive 2003/99/EC, which obliges EU MSs to collect relevant and, where applicable, comparable
1
Commission Implementing Decision 2013/652/EU of 12 November 2013 on the monitoring and reporting of antimicrobial
resistance in zoonotic and commensal bacteria. OJ L 303, 14.11.2013, p. 2639.
2
Decision No 1082/2013/EU of the European Parliament and of the Council of 22 October 2013 on serious cross-border threats
to health and repealing Decision No 2119/98/EC. OJ L 293, 5.11.2013, p. 115.
3
Commission Decision 2012/506/EU amending Decision 2002/253/EC laying down case definitions for reporting communicable
diseases to the Community network under Decision No 2119/98/EC of the European Parliament and of the Council. OJ L 262,
27.9.2012, p. 157.
4
Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general
principles and requirements of food law, establishing the EFSA and laying down procedures in matters of food safety. OJ L 31,
1.2.2002, p. 124.
5
Regulation (EC) No 851/2004 of the European Parliament and of the Council of 21 April 2004 establishing a European centre
for disease prevention and control. OJ L 142, 30.4.2004, p. 111.
data on zoonoses, zoonotic agents, AMR and food-borne outbreaks. In addition, MSs are required to
assess trends and sources of these agents, as well as outbreaks in their territory, submitting an
annual report each year by the end of May to the EC covering the data collected. EFSA is assigned the
tasks of examining these data and publishing the EU annual Summary Reports. In accordance with
Article 9 of the Zoonoses Directive 2003/99/EC, EFSA shall examine the submitted national reports of
the EU MSs and publish by the end of November a summary report on the trends and sources of
zoonoses, zoonotic agents and AMR in the EU.
1. Introduction
The antimicrobial agents used in food-producing animals in Europe are frequently the same, or belong
to the same classes, as those used in human medicine. Antimicrobial resistance (AMR) is the main
undesirable side effect of antimicrobial use in both humans and animals, and results from the
continuous positive selection of resistant bacterial clones, whether these are pathogenic, commensal
or even environmental bacteria. This will modify the population structure of microbial communities,
leading to accelerated evolutionary trends with unpredictable consequences for human and animal
health. Both the route of administration and the administered quantities of antimicrobials may differ
between humans and food-producing animals; moreover, there are important variations between and
within food-producing animal populations, as well as between countries.
Bacterial resistance to antimicrobials occurring in food-producing animals can spread to people not
only via food-borne routes, but also by routes such as water or other environmental contamination, as
well as through direct animal contact. Campylobacter, Salmonella and some strains of Escherichia coli
are examples of zoonotic bacteria which can infect people by the food-borne route. Infections with
bacteria which are resistant to antimicrobials may result in treatment failures or necessitate the use of
second-line antimicrobials for therapy. The commensal bacterial flora can also form a reservoir of
resistance genes, which may be transferred between bacterial species, including organisms capable of
causing disease in both humans and animals (EFSA, 2008).
The monitoring of AMR in zoonotic and commensal bacteria in food-producing animals and food
thereof is a prerequisite for understanding the development and diffusion of resistance, providing
relevant risk assessment data, and evaluating targeted interventions. Resistance monitoring entails
specific and continuous data collection, analysis and reporting and enables to follow temporal trends
in the occurrence and distribution of resistance to antimicrobials. Resistance monitoring should also
allow for the identification of emerging or specific patterns of resistance.
6
Commission Implementing Decision 2013/652/EU of 12 November 2013 on the monitoring and reporting of antimicrobial
resistance in zoonotic and commensal bacteria. OJ L 303, 14.11.2013, p. 2639.
7
The epidemiological cut-off (ECOFF) values separate the naive, susceptible wild-type bacterial populations from isolates that
have developed reduced susceptibility to a given antimicrobial agent (Kahlmeter et al., 2003). The ECOFFs may differ from
breakpoints used for clinical purposes, which are defined against a background of clinically relevant data, including
therapeutic indication, clinical response data, dosing schedules, pharmacokinetics and pharmacodynamics. The use of
harmonised methods and ECOFFs ensures the comparability of data over time at the country level and also facilitated the
comparison of resistance between MSs.
guide the susceptibility testing required for EU surveillance and reporting to ECDC. Consultation was
also sought from EFSA, EUCAST and the EURL-AR to facilitate comparison of data between countries
and with results from the AMR monitoring performed in isolates from animals and from food products.
The protocol is effective from 2014 and supports the implementation of the Commission Action Plan
on AMR. One of the recommendations is that, for the purpose of the joint report with EFSA, human
data should also be interpreted based on ECOFFs. As this requires quantitative data, ECDC introduced
quantitative antimicrobial susceptibility testing (AST) data reporting in last years data collection and
encourages countries to use it. As the EU protocol is not a legal document but a recommendation and
joint agreement, it is up to each National Public Health Reference Laboratory whether to adapt to the
protocol. Most laboratories did adopt the new priority panel of antimicrobials suggested in the
protocol, in 2014, whereas the optional antimicrobials were tested by fewer laboratories. The
proposed testing algorithm for screening and confirmation of extended spectrum beta-lactamase
(ESBL)-producing Salmonella spp., including detection of pAmpC, however, does not seem to have
been implemented or at least not reported to ECDC as planned.
Since the majority of laboratories use disk diffusion for AST, ECDC set up a joint project with EUCAST
to establish inhibition zone diameter ECOFFs for C. jejuni, C. coli and Salmonella spp. New disk
diffusion ECOFFs were established for nine antimicrobials for Salmonella spp. in 2014 (Matuschek et
al., 2015), whereas the project is still ongoing for C. jejuni and C. coli.
External quality assurance to support laboratories in implementing the recommended test methods
and antimicrobials and obtaining high-quality AST results is provided by Statens Serum Institute in
Denmark through a contract with ECDC.
report. The serovars presented in the report are S. Enteritidis, S. Infantis, S. Kentucky, S. Derby,
S. Typhimurium and monophasic S. Typhimurium. Additional serovars among the ten most common in
human cases in 2014 or serovars of particular interest due to recent outbreaks etc. are available in
appendices (S. Bovismorbificans, S. Bredeney, S. Chester, S. Hadar, S. Indiana, S. Mbandaka,
S. Muenchen, S. Newport, S. Paratyphi B var. L+ tartrate+ (var. Java), S. Rissen, S. Senftenberg,
S. Stanley and S. Virchow). The proportion of resistant isolates are only shown when at least 20
isolates of Salmonella spp. or at least 10 isolates of separate serovars were tested in that MS.
In order to better assess the impact from food consumed within each reporting country on the AMR
levels found in human Salmonella isolates, the analysis focused on domestically acquired cases.
However, as several countries had not provided any information on travel (or non-travel) of their
cases, cases with unknown travel status were also included in addition to domestically acquired cases.
The proportions of travel-associated, domestic and unknown cases among the tested Salmonella
isolates are presented in Table SALMTRAVHUM.
Multidrug resistance (MDR) of human Salmonella spp. to nine antimicrobial classes was analysed. For
the 2014 report, ECDC and EFSA agreed to include the same antimicrobial classes in the MDR analysis
for better comparison between the two sectors. For the human data analysis, this meant including
also carbapenems which had not been possible in 2013 when too few countries reported on this class.
Multidrug resistance of an isolate was defined as resistance or non-susceptibility to at least three
different antimicrobial classes (Magiorakos et al., 2012). The antimicrobials included were ampicillin,
cefotaxime/ceftazidime, chloramphenicol, ciprofloxacin/pefloxacin/nalidixic acid, gentamicin,
meropenem, sulfonamides/sulfamethoxazole, tetracyclines and trimethoprim/sulfamethoxazole (co-
trimoxazole). Resistance to nalidixic acid, ciprofloxacin and pefloxacin were addressed together, as
they belong to the same class of antimicrobials: quinolones. Isolates that were resistant or non-
susceptible to any of these antimicrobials were classified as resistant or non-susceptible to the class of
quinolones. The same method was applied to the two third generation cephalosporins cefotaxime and
ceftazidime. Trimethoprim and co-trimoxazole were also addressed together since a few countries had
only tested for susceptibility to the combination. This approach was considered appropriate because
among the eight countries that provided data on both trimethoprim alone and the combination co-
trimoxazole, the proportion of resistant or non-susceptibles corresponded closely between the two.
Co-resistance to ciprofloxacin and cefotaxime was also analysed as these two antimicrobials are
considered the most important for treatment of severe salmonellosis (ECDC et al., 2009). Both
microbiological co-resistance (using EUCAST ECOFFs) and clinical co-resistance (using EUCAST
CBPs) were determined.
For the first time, the proportions of human isolates resistant to ciprofloxacin, nalidixic acid and
cefotaxime were also presented in maps to provide an overview of the spatial distribution of
resistance. Data were only shown for countries reporting at least 10 isolates.
Table 3: Antimicrobials reported, methods used, type of data reported and interpretive criteria applied by MSs for human Salmonella AST data in 2014
Chloramphenicol
Trimethoprim-
Ciprofloxacin/
Trimethoprim
Sulfonamides
Nalidixic acid
Tetracyclines
Azithromycin
Quantitative (Q)
Ceftazidime
Meropenem
Cefotaxime
Gentamicin
Tigecycline
Method Interpretive
pefloxacin
Country Ampicillin or
used criteria
Colistin
categorical (SIR)
sulfa
Austria DD Q Interpreted by ECDC. EUCAST ECOFFs 2014 for all except CLSI CBP
2014 for SUL
Belgium DD SIR No update. In 2013, EUCAST CBP 2013 (AMP, CTX, CHL, GEN, SXT),
CLSI CBP 2013 (CIP, NAL, SUL, TET)
Denmark DL Q Interpreted by ECDC, as for Austria. EFSA criteria for AZM MIC
Estonia DD Q Interpreted by ECDC, as for Austria
Finland DD Q Interpreted by ECDC, as for Austria
France DD/DL(a) SIR CA-SFM CBP 2013
Greece DD Q Interpreted by ECDC, as for Austria
Hungary DD/DL(a) SIR EUCAST CBP 2014 except CLSI CBP 2014 for NAL, SUL and TCY
Ireland DL Q Interpreted by ECDC, as for Austria. EFSA criteria for AZM MIC
Italy DD Q Interpreted by ECDC, as for Austria
Latvia DD SIR CLSI and EUCAST CBP
Lithuania DD SIR No update provided. Earlier CLSI
Luxembourg DD/DL(a) Q Interpreted by ECDC, as for Austria
Malta (b) DL SIR Biomerieux Vitek II system; follows EUCAST CBP 2014
Netherlands DL Q Interpreted by ECDC, as for Austria. EFSA criteria for AZM MIC
Norway DD Q Interpreted by ECDC, as for Austria
Portugal DD Q Interpreted by ECDC, as for Austria
Romania DD Q Interpreted by ECDC, as for Austria
Slovakia (b) DD/DL SIR No update provided. In 2013, EUCAST CBP 2013 except CLSI CBP
2013 for NAL, SUL and TCY
Slovenia DD/DL(a) SIR EUCAST CBP 2014 except CLSI CBP 2014 for SUL and TET.
Spain DD SIR EUCAST CBP 2014 except CLSI CBP 2010 for NAL and TET
United DL(c) SIR No update provided. Earlier HPA methodology based on Frost 1994
Kingdom
MSs: Member States; AST: antimicrobial susceptibility testing; DD: disk diffusion; DL: dilution; Q: quantitative data; SIR: susceptible, intermediate, resistant (categorical data); ECDC: European
Centre for Disease Prevention and Control; EUCAST: European Committee on Antimicrobial Susceptibility Testing; ECOFF: epidemiological cut-off; CLSI: Clinical and Laboratory Standards
Institute; CBP: clinical breakpoint; SUL: sulfonamides; AMP: ampicillin; CTX: cefotaxime; CHL: chloramphenicol; GEN: gentamicin; SXT: sulfamethoxazole; CIP: ciprofloxacin; NAL: nalidixic acid;
TET: tetracycline; AZM: azithromycin; TCY: tigecycline; CA-SFM: French Society for Microbiology; HPA: Health Protection Agency (UK).
(a): Gradient strip.
(b): All gentamicin results for Salmonella automatically reported as resistant and therefore excluded.
(c): In agar breakpoint.
Resistance levels differ quite substantially between the two most important Campylobacter species, C.
jejuni and C. coli, and data are therefore presented by species. The proportion of resistant isolates is
only shown when at least 10 isolates were reported from a MS.
In order to better assess the impact from food consumed within each reporting country on the
antimicrobial resistance levels found in human Campylobacter isolates, the analysis focused on
domestically acquired cases. However, as several countries had not provided any information on travel
(or non-travel) of their cases, cases with unknown travel status were included in the analysis. The
proportions of travel-associated, domestic and unknown cases among the tested Campylobacter
isolates are presented in Table CAMPTRAVHUM.
Multidrug resistance of a C. jejuni or C. coli isolate was defined as resistance or non-susceptibility to at
least three different antimicrobial classes (Magiorakos et al., 2012). For the 2014 report, the
antimicrobials in the MDR analysis were harmonised between EFSA and ECDC and included
ciprofloxacin, erythromycin, gentamicin and tetracyclines. Co-resistance to ciprofloxacin and
erythromycin was also analysed, as these two antimicrobials are considered the most important for
treatment of severe campylobacteriosis (ECDC, EFSA, EMEA and SCENIHR 2009). Both
microbiological co-resistance (using EUCAST ECOFFs) and clinical co-resistance (using EUCAST
CBPs) were determined.
For the first time, the proportion of human isolates resistant to erythromycin and ciprofloxacin were
also presented in maps to provide an overview of the spatial distribution of resistance. Data were only
shown for countries reporting at least 10 isolates.
Table 4: Antimicrobials reported, method used, type of data reported and interpretive criteria
applied by MSs for human Campylobacter AST data in 2014
Co-amoxiclav
Erythromycin
Ciprofloxacin
Tetracyclines
Gentamicin
Type
Method Interpretive
Country of
used criteria
data
Austria DL Q
Interpreted by ECDC. EUCAST ECOFF (CIP, ERY,
GEN MIC, TET), CA-SFM CBP 2014 (AMC, GEN DD)
Estonia DD Q Interpreted by ECDC, as for Austria
France DD SIR In 2013, EUCAST CBP 2013 (CIP, ERY, TET),
CA-SFM CBP 2013 (AMC, GEN)
Italy DD Q Interpreted by ECDC, as for Austria
Lithuania DD SIR No information
Luxembourg DD/DL(a) Q Interpreted by ECDC, as for Austria
Malta DL/DL(a)/DD SIR EUCAST CBP 2014 (CIP, ERY)
Netherlands DD/DL SIR Survey in 12 clinical labs in NL in 2009
(Ned Tijdschr Med Microbiol 2009;17:nr1)
Norway DL(a) Q Interpreted by ECDC, as for Austria
Portugal DD Q Interpreted by ECDC, as for Austria
Romania DD Q Interpreted by ECDC, as for Austria
Slovakia DL SIR In 2013, CLSI CBP
Slovenia DD Q Interpreted by ECDC, as for Austria
Spain DL(a) SIR EUCAST CBP 2014 (CIP, ERY, TET), CA-SFM CBP
2014 (AMC, GEN)
MSs: Member States; AST: antimicrobial susceptibility testing; DD: disk diffusion; DL: dilution; Q: quantitative data; SIR:
susceptible, intermediate, resistant (categorical data); ECDC: European Centre for Disease Prevention and Control; EUCAST:
European Committee on Antimicrobial Susceptibility Testing; ECOFF: epidemiological cut-off; CIP: ciprofloxacin; ERY:
erythromycin; GEN: gentamicin; MIC: minimum inhibitory concentration; TET: tetracycline; CA-SFM: French Society for
Microbiology; CBP: clinical breakpoint; AMC: amoxicillin/clavulanate; TCY: tigecycline.
(a): Gradient strip.
Salmonella
In 2014, representative Salmonella isolates for monitoring AMR were collected by MSs from
populations of laying hens, broilers and fattening turkeys sampled within the framework of the
Salmonella National Control Programmes (NCPs), established in accordance with Article 5(1) of
Regulation (EC) No 2160/2003, as well as from carcases of both broilers and fattening turkeys sample
for testing and verification of compliance, in accordance with point 2.1.5 of Chapter 2 of Annex 1 to
Regulation (EC) No 2073/2005. Not more than one isolate per Salmonella serovar from the same
epidemiological unit (flock of birds) per year should be included in the AMR monitoring. In most MSs,
the isolates tested for antimicrobial susceptibility constituted a representative subsample of the total
Salmonella isolates available at the National Reference Laboratory (NRL) and/or other laboratories
involved, obtained in a way that ensured geographical representativeness and even distribution over
the year. Conversely, in the case of low prevalence, all the Salmonella isolates available should be
tested for susceptibility.
8
Quantitative data derived from dilution methods consisted of the number of isolates having a specific MIC value (measured
in mg/L) relative to the total number of isolates tested, for each antimicrobial agent and specific food/animal category.
MRSA
Isolates may have been collected by different monitoring approaches, either by active monitoring of
animals and foods or, in some cases, by passive monitoring based on diagnostic submission of
samples from clinical cases of disease in animals, or from foods sampled as part of investigatory work.
Both specific monitoring programms were voluntary. For the specific monitoring of ESBL-/AmpC-
/carbapenemase-producing E. coli, the method started with a non-selective pre-enrichment step,
followed by inoculation on McConkey agar containing a third-generation cephalosporin in a selective
concentration, in accordance with the most recent version of the detailed protocol for standardisation
of the EURL-AR.10 Using this protocol, also carbapenemase-producing isolates could be recovered. For
the specific monitoring of carbapenemase-producing microorganisms, isolation required the use of
non-selective pre-enrichment and subsequent selective plating on carbapenem-containing media, in
accordance with the most recent version of the detailed protocol of the EURL-AR.
The microbial species was identified using an appropriate method. If available, one presumptive ESBL-
/AmpC-/carbapenemase-producing E. coli isolate obtained from each positive caecal sample and meat
sample was tested for resistance to the first panel of antimicrobials (Table 5) and then submitted for
extended susceptibility testing if they are resistant to cefotaxime, ceftazidime or meropenem, based
on the interpretative criteria (epidemiological cut-off values).
All presumptive ESBL-/AmpC-/carbapenemase-producing E. coli isolates, identified through selective
plating were further tested with the second panel of antimicrobials (Table 7) to phenotypically verify
presumptive ESBL-/AmpC-/carbapenemase-producers.
9
The same sampling design was used to collect indicator E. coli isolates, whether dedicated to the routine monitoring of AMR or
the specific monitoring of ESBL-/AmpC-/carbapenemase-producing E. coli.
10
Available online: www.crl-ar.eu
Table 5: Panel of antimicrobial substances included in AMR monitoring, EUCAST ECOFFs and
concentration ranges tested in Salmonella spp. and indicator commensal E. coli (first
panel)
Table 6: Panel of antimicrobial substances included in AMR monitoring, EUCAST ECOFFs and
concentration ranges tested in C. jejuni and C. coli
Table 7: Panel of antimicrobial substances, EUCAST ECOFFs and concentration ranges used for
testing only Salmonella spp. and indicator commensal E. coli isolates resistant to
cefotaxime, ceftazidime or meropenem (second panel)
Data description
Throughout the report, level or occurrence of AMR means the percentage of resistant isolates as a
proportion of the isolates tested of that microorganism. MSs reporting group means the MSs that
provided data and were included in the relevant table of antimicrobial resistance for that
bacteriumfood or animal categoryantimicrobial combination. Terms used to describe the levels
or occurrence of antimicrobial resistance are rare: < 0.1%, very low: 0.1% to 1.0%, low: > 1%
to 10.0%, moderate: > 10.0% to 20.0%, high: > 20.0% to 50.0%, very high: > 50.0% to
70.0%, extremely high: > 70.0%. Although these terms are applied to all antimicrobials, the
significance of a given level of resistance depends on the particular antimicrobial and its
importance in human and veterinary medicine.
11
Giving the percentage of isolates microbiologically resistant out of those tested.
12
More than 10 isolates tested by a MS and more than four MSs reporting results for that antimicrobial, microorganism, food or
animal category.
over time were visually explored by trellis graphs, using the lattice package in the R software (R
version 2.14.2 (29/2/2012)).
In order to assess the statistical significance of temporal trends, the proportions of resistance were
modelled against time in a logistic regression. This analysis was carried out using the PROC LOGISTIC
of SAS 9.2 for each country where there were 5 years or more of available data to use in the model.
The PROC LOGISTIC function uses a logit transform to model the proportion of prevalence against
year, and provides estimates for both intercepts and slope. Models where the likelihood ratio test
suggested it to be meaningful and resulting in a p-value associated with slope of < 0.05 were
considered to be significant.
Definitions
For the purpose of this analysis, a multiresistant isolate is one defined as resistant to at least three
different antimicrobial substances, belonging to any three antimicrobial families listed in the
harmonised set of antimicrobials included in the Decision 2013/652/EU. Table 5: and Table 6: list
those recommended antimicrobials. Resistance to nalidixic acid and resistance to ciprofloxacin, as well
as the resistance to cefotaxime and to ceftazidime are respectively addressed together.
In contrast, a fully susceptible isolate is one defined as non-resistant to all of the antimicrobial
substances included in the harmonised set of substances for Salmonella, Campylobacter and indicator
E. coli.
The term co-resistance has been defined as two or more resistance genes which are genetically
linked, i.e. located adjacent or close to each other on a mobile genetic element (Chapman, 2003). For
brevity, the term is used slightly more loosely in this report and indicates two or more phenotypic
resistances to different classes of antimicrobials, exhibited by the same bacterial isolate.
MDR patterns
The frequency and percentage of isolates exhibiting various MDR patterns considering the
antimicrobials tested were determined for Salmonella (Salmonella spp., S. Enteritidis, S. Typhimurium
and monophasic S. Typhimurium), Campylobacter species and indicator E. coli for each country and
each animal population/food category. Isolates for which no susceptibility data were provided for
some of the antimicrobial substances were disregarded. Data analysis was presented for a particular
country only when the number of tested isolates was at least 10, except for allSalmonella serovars.
synergy). In this case, the cefepime/clavulanic acid synergy test should be used to overturn/confirm
the presence of ESBLs in these isolates (EUCAST, 2013), but unfortunately, the combination
cefepime/clavulanic acid was not included among the substances tested for the monitoring. The
inclusion of resistance to cefepime with a MIC value 4 mg/L, as an additional criteria proposed
elsewhere (EFSA, 2012), could be useful to ascertain the presence of an ESBLproducer.
For the present report, isolates with MICs > 1 mg/L for cefotaxime and/or ceftazidime, positive
synergy tests for any of these antimicrobials/clavulanic acid and cefoxitin MIC > 8 mg/L, were
considered as putative ESBL- and AmpC-producers and were classified under the ESBL/AmpC-
phenotype category.
For the classification of isolates into the putative carbapenem producers (CPs), a meropenem
screening cut-off of > 0.12 mg/L (which coincides with the harmonised ECOFF) was chosen. It is
known that other mechanisms (i.e. hyperproduction or combination of ESBLs and/or AmpC and porin
loss) can also affect to the MIC values generated for the different carbapenems, especially for
ertapenem. The confirmation of the carbapemase production recommended by the EUCAST guidelines
cannot be inferred from the carbapenem susceptibility testing data reported, but needs further
phenotypic or molecular testing. Those MS which reported data suggesting the presence of putative
CPs were recommended to validate the results by performing further confirmatory testing, and the
EURL-AR offered to apply whole genome sequencing of the isolates. For the present report, isolates
with MIC > 0.12 mg/L for meropenem would be considered as putative CP and were classified under
the CP-phenotype. Isolates with a MIC > 0.12 for ertapenem and/or MIC > 1 mg/L for imipenem
(EUCAST screening cut-offs, one dilution step higher than the currently defined ECOFFs) but no
resistance to meropenem (MIC < 12 mg/L) were classified under the category other phenotype.
Finally, isolates with MICs 1 mg/L for cefotaxime and ceftazidime would be considered as not ESBL-
and/or AmpC producers. This implied that some isolates considered microbiologically resistant (MICs
over the ECOFFS) would not be further classified, as probably other mechanisms or technical issues in
the MIC testing (i.e. MIC value close to the ECOFF) would be responsible for the MIC values obtained.
For the present report, cefotaxime- and ceftazidime-resistant isolates with MICs 1 mg/L for both
antimicrobials were considered as putative non ESBL/AmpC-producers and were classified under the
category other phenotype.
We are aware that without a further molecular characterisation of the isolates, it will not be possible
to know exactly which resistance mechanisms are present. For epidemiological purposes and based on
the EUCAST guidelines, the classification of putative producers for the different mechanism
conferring resistance to third-generation cephalosporins and/or carbapenems was considered.
3. Assessment
For 2014, 21 MSs and Norway provided data on AMR in human Salmonella isolates. Twelve countries
(Austria, Denmark, Estonia, Finland, Greece, Ireland, Italy, Luxembourg, the Netherlands, Norway,
Portugal and Romania) reported isolate-based AST results as measured values (inhibition zone
diameters or MICs) which was five countries more than for 2013. Ten countries reported case-based
AST results interpreted as susceptible (S), intermediate (I) or resistant (R) according to the CBPs
applied (Table SALMOVERVIEW). Twenty-seven MSs and two non-MSs (Iceland and Norway) reported
quantitative MIC data on the AMR of Salmonella isolates recovered from animals and food in 2014
(Table SALMOVERVIEW).
13
SIR stands for susceptible, intermediate, resistant.
N: total number of isolates tested for susceptibility against the whole common antimicrobial set for Salmonella; sus: susceptible
to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one up to nine antimicrobial classes of
the common set for Salmonella.
Figure 8: Frequency distribution of Salmonella spp. isolates from humans completely susceptible or
resistant to one to eight antimicrobial classes in 2014
Table 8: Antimicrobial resistance in Salmonella spp. (all non-typhoidal serovars) from humans per country in 2014
N: total number of isolates tested for susceptibility against the whole common antimicrobial set for Salmonella; sus: susceptible
to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one up to nine antimicrobial classes of
the common set for Salmonella.
Table 9: Antimicrobial resistance in Salmonella Enteritidis from humans per country in 2014
Figure 10: Spatial distribution of ciprofloxacin resistance among S. Enteritidis from human cases in
reporting countries in 2014
Figure 11: Spatial distribution of nalidixic acid resistance among S. Enteritidis from human cases in
reporting countries in 2014
Figure 12: Spatial distribution of cefotaxime resistance among S. Enteritidis from human cases in
reporting countries in 2014
N: total number of isolates tested for susceptibility against the whole common antimicrobial set for Salmonella; sus: susceptible
to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one up to nine antimicrobial classes of
the common set for Salmonella.
Figure 13: Frequency distribution of Salmonella Infantis isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014
Table 10: Antimicrobial resistance in Salmonella Infantis from humans per country in 2014
Figure 14: Spatial distribution of ciprofloxacin resistance among S. Infantis from human cases in
reporting countries in 2014
Figure 15: Spatial distribution of nalidixic acid resistance among S. Infantis from human cases in
reporting countries in 2014
Figure 16: Spatial distribution of cefotaxime resistance among S. Infantis from human cases in
reporting countries in 2014
N: total number of isolates tested for susceptibility against the whole common antimicrobial set for Salmonella; sus: susceptible
to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one up to nine antimicrobial classes of
the common set for Salmonella.
Figure 17: Frequency distribution of Salmonella Kentucky isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014
Table 11: Antimicrobial resistance in Salmonella Kentucky from humans per country in 2014
Table 12: Antimicrobial resistance in Salmonella Derby from humans per country in 2014
N: total number of isolates tested for susceptibility against the whole common antimicrobial set for Salmonella; sus: susceptible
to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one up to nine antimicrobial classes of
the common set for Salmonella.
Figure 18: Frequency distribution of Salmonella Typhimurium isolates from humans completely
susceptible or resistant to one to nine antimicrobial classes in 2014
14
This pattern of MDR (resistance to ampicillin, sulfonamide and tetracycline) typically also includes resistance to streptomycin;
however, as described in the Materials and methods section, data on this antimicrobial are no longer included in this report.
important antimicrobials was 1.1% for ciprofloxacin and 0.8% for cefotaxime, with the highest levels
of ciprofloxacin resistance in Ireland (9.4%) and of cefotaxime resistance in Austria (1.5%) and Spain
(1.3%).
N: total number of isolates tested for susceptibility against the whole common antimicrobial set for Salmonella; sus: susceptible
to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one up to nine antimicrobial classes of
the common set for Salmonella.
ciprofloxacin, nalidixic acid, sulfamethoxazole and tetracycline ranged from low to extremely high
(1.297.9%) in Salmonella spp. from broiler meat in most of the reporting MSs, whereas no resistance
was recorded in Ireland. Resistance to ampicillin was generally low to moderate in most reporting MSs
(4.314.0%), although high levels were also observed in two MSs and three MSs did not register any
resistance. Overall resistance to gentamicin (0.7%) and chloramphenicol (2.2%) remained at low
levels. Resistance was not detected or low levels of resistance to azithromycin, colistin and tigecycline
were reported by most MSs (027.7%). Microbiological resistance to cefotaxime and ceftazidime was
recorded by only two MSs at very low or low levels.
Ireland (N=21)
France (N=169)
Lithuania (N=6) sus
Czech Republic (N=50) res1
res2
Germany (N=41)
res3
Belgium (N=81)
res4
Austria (N=24) res5
Poland (N=31) res6
Slovakia (N=57) res7
Spain (N=130) res8
res9
Slovenia (N=15)
Hungary (N=47)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 20: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobial classes in Salmonella spp. from broiler meat in MSs in 2014
comparable to most other reporting MSs. In contrast to S. Enteritis, a very high proportion of isolates
(83.1%) were multiresistant (79.5100%) (Table COMINFANBRMEAT).
Out of 69 isolates of S. Indiana tested, only two isolates were found resistant: one only to
ciprofloxacin and one to colistin and tetracycline (Table INDIANABRMEATD).
sus
France (N=173)
res1
res2
Figure 21: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobial classes in Salmonella spp. from fattening turkey meat in MSs in 2014
Table 13: Occurrence of resistance to selected antimicrobials in Salmonella spp. isolates from meat from broilers and meat from fattening turkeys in 2014
Country Ampicillin Azithromycin Cefotaxime Ceftazidime Chloramphenicol Ciprofloxacin Colistin (a)
N % Res N % Res N % Res N % Res N % Res N % Res N % Res
Meat from broilers
Austria 24 0 24 0 24 0 24 0 24 0 24 62.5 24 0
Belgium 81 23.5 81 6.2 81 3.7 81 2.5 81 4.9 81 43.2 81 3.7
Czech Republic 50 0 50 0 50 0 50 0 50 0 50 24 50 14.0
France 169 5.9 169 1.2 169 0 169 0 169 0.6 169 1.2 169 2.4
Germany 41 12.2 41 2.4 41 0 41 0 41 4.9 41 29.3 41 7.3
Hungary 47 4.3 47 0 47 0 47 0 47 0 47 97.9 47 0
Ireland 28 0 27 0 27 0 28 0 25 0 29 0 27 0
Poland 31 29.0 31 0 31 0 31 0 31 0 31 64.5 31 0
Slovakia 57 14.0 57 0 57 0 57 0 57 0 57 70.2 57 3.5
Slovenia 15 6.7 15 0 15 0 15 0 15 0 15 93.3 15 0
Spain 130 6.9 130 5.4 130 0.8 130 0.8 130 6.2 130 70 130 13.8
Total (MSs 11) 673 9.4 672 2.2 672 0.6 673 0.4 670 2.2 674 42.6 672 5.5
Meat from fattening turkeys
France 173 24.3 173 0 173 0 173 0 173 10.4 173 6.9 173 38.7
Germany 31 64.5 31 6.5 31 0 31 0 31 0 31 74.2 31 0
Hungary 22 27.3 22 0 22 0 22 0 22 0 22 90.9 22 0
Total (MSs 3) 226 30.1 226 0.9 226 0 226 0 226 8 226 24.3 226 29.6
France (N=36)
Ireland (N=14)
Greece (N=20)
Czech Republic (N=212)
Denmark (N=26)
United Kingdom (N=168)
Iceland (N=16) sus
Germany (N=28) res1
Austria (N=113) res2
Netherlands (N=88) res3
Portugal (N=51)
res4
Italy (N=66)
res5
Croatia (N=126)
Cyprus (N=45) res6
Poland (N=85) res7
Slovakia (N=20) res8
Belgium (N=170) res9
Romania (N=553)
Spain (N=135)
Hungary (N=169)
Slovenia (N=85)
Bulgaria (N=17)
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 22: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from broilers in MSs in 2014
Figure 23: Spatial distribution of ciprofloxacin resistance among Salmonella spp. from broilers in
countries reporting MIC data in 2014
Figure 24: Spatial distribution of nalidixic acid resistance among Salmonella spp. from broilers in
countries reporting MIC data in 2014
Figure 25: Spatial distribution of cefotaxime resistance among Salmonella spp. from broilers in
countries reporting MIC data in 2014
Table 14: Occurrence of resistance to selected antimicrobials in Salmonella spp. isolates from broilers in 2014, using harmonised ECOFFs
Denmark (N=7)
Spain (N=1)
France (N=4)
Iceland (N=7)
Netherlands (N=10)
Germany (N=10) sus
Belgium (N=11) res1
Cyprus (N=20) res2
Czech Republic (N=41) res3
Italy (N=33) res4
Austria (N=56) res5
Romania (N=317) res6
Bulgaria (N=10) res7
Hungary (N=125)
Poland (N=17)
Slovakia (N=13)
Slovenia (N=71)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 26: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Infantis from broilers in MSs in 2014
Figure 27: Spatial distribution of ciprofloxacin resistance among Salmonella Infantis from broilers in
countries reporting MIC data in 2014
Figure 28: Spatial distribution of nalidixic acid resistance among Salmonella Infantis from broilers in
countries reporting MIC data in 2014
Figure 29: Spatial distribution of cefotaxime resistance among Salmonella Infantis from broilers in
countries reporting MIC data in 2014
Austria (N=16)
Denmark (N=1)
France (N=1)
Germany (N=1) sus
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 30: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Enteritidis from broilers in MSs in 2014
Figure 31: Spatial distribution of ciprofloxacin resistance among Salmonella Enteritidis from broilers
in countries reporting MIC data in 2014
Figure 32: Spatial distribution of nalidixic acid resistance among Salmonella Enteritidis from broilers
in countries reporting MIC data in 2014
Figure 33: Spatial distribution of cefotaxime resistance among Salmonella Enteritidis from broilers in
countries reporting MIC data in 2014
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 34: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Kentuky from broilers in MSs in 2014
Resistance levels in S. Typhimurium and monophasic S. Typhimurium isolates from broiler flocks
Resistance levels to ampicillin, sulfamethoxazole and tetracycline (overall 33.342.5%) in
S. Typhimurium isolates from broilers (Table TYPHIBRD) were found to mainly be high to extremely
high. Chloramphenicol resistance varied from none to 100% (overall 16.1%), whereas resistance to
gentamicin was reported by only one MS. Resistance to cefotaxime and ceftazidime was reported only
by Belgium, whereas nalidixic acid and ciprofloxacin resistance varied markedly between MSs from
none to 100% (Romania). In broilers, 32.5% (17 MSs, N=83) of the S. Typhimurium isolates were
multiresistant. Microbiological co-resistance to ciprofloxacin and cefotaxime was only reported for one
isolate by Belgium (Tables COMTYPHIBR).
Resistance levels to ampicillin, sulfamethoxazole and tetracycline (overall 79.482.4%) in
monophasic S. Typhimurium isolates from broilers (Table MONTPHIYBRD) were found to mainly
be high to extremely high. Chloramphenicol resistance was registered only by Malta (50.0%), whereas
resistance to gentamicin was reported only by the United Kingdom. Resistance to cefotaxime and
ceftazidime was reported only by Malta (50.0%) and the Netherlands (20.0%), whereas nalidixic acid
and ciprofloxacin resistance was reported only by Belgium. In broilers, 74.2% (eight MSs, N=31) of
the monophasic S. Typhimurium isolates were multiresistant. Microbiological co-resistance to
ciprofloxacin and cefotaxime was not reported. (Tables COMMONTYPHIBR).
Table 15: Occurrence of resistance to selected antimicrobials in Salmonella Enteritidis isolates from broilers in 2014
Table 16: Occurrence of resistance to selected antimicrobials in Salmonella Infantis isolates from broilers in 2014, using harmonised ECOFFs
Slovenia (N=15)
Netherlands (N=44)
United Kingdom (N=53)
France (N=86)
Croatia (N=19) sus
res1
Germany (N=80)
res2
Hungary (N=57)
res3
Poland (N=45)
res4
Greece (N=43)
res5
Spain (N=138)
res6
Portugal (N=38) res7
Austria (N=45) res8
Italy (N=81) res9
Cyprus (N=17)
Romania (N=46)
Belgium (N=29)
0% 20% 40% 60% 80% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the EFSA common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 35: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from laying hens in MSs in 2014
Spatial trends in resistance among Salmonella spp. from laying hen flocks
The levels of resistance to ciprofloxacin in Salmonella spp. from laying hens were high in some MSs
from Eastern and Southern Europe (Cyprus, Hungary, Italy and Romania), and low to moderate in
other reporting MSs (Figure 36). The levels of resistance to nalidixic acid were very similar to the
levels of resistance to ciprofloxacin (Figure 37). Low level of resistance to cefotaxime was reported
only by France, Poland and Romania, whereas no resistance was reported from other 13 MSs across
Europe (Figure 38).
Figure 36: Spatial distribution of ciprofloxacin resistance among Salmonella spp. from laying hens in
countries reporting MIC data in 2014
Figure 37: Spatial distribution of nalidixic acid resistance among Salmonella spp. from laying hens in
countries reporting MIC data in 2014
Figure 38: Spatial distribution of cefotaxime resistance among Salmonella spp. from laying hens in
countries reporting MIC data in 2014
50
25
0
Germany Hungary Ireland Italy Latvia
100
75
% Resistant isolates
50
25
0
Netherlands Poland Portugal Slovakia Slovenia
100
75
50
25
0
Spain United Kingdom
100
75
50
25
0
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
Year
A statistically significant trend for 5 or more years, as tested by a logistic regression model (p 0.05), was observed for
ciprofloxacin and nalidixic acid in Austria (), Belgium (), Germany (), Italy (), Slovakia (), Slovenia (), for ampicillin in
Belgium (), the Czech Republic (), Denmark (), Italy () , the Netherlands (), Slovakia (), Slovenia (), Spain () and the
United Kingdom (), for ciprofloxacin in Portugal (), for cefotaxime in Belgium (), the Czech Republic (), France (), Germany
(), Italy () and the Netherlands (). A statistically significant trend was observed for ciprofloxacin in Portugal (), for nalidixic
acid in Portugal () and Spain ().
Figure 39: Trends in ampicillin, cefotaxime, ciprofloxacin and nalidixic acid resistance in tested
Salmonella spp. isolates from Gallus gallus in reporting MSs, 20082014, quantitative
data
50
25
0
Germany Hungary Italy Latvia
100
75
% Resistant isolates
50
25
0
Netherlands Poland Portugal Slovakia
100
75
50
25
0
Spain
100
75
50
25
0
2008
2009
2010
2011
2012
2013
2014
Year
A statistically significant trend for 5 or more years, as tested by a logistic regression model (p 0.05), was observed in the
Czech Republic (), France (), Poland () and Portugal () for both ciprofloxacin and nalidixic acid, for ampicillin in France ()
and Portugal (), for ciprofloxacin in Italy () and for cefotaxime in the Netherlands () and Portugal ().
Figure 40: Trends in ampicillin, cefotaxime, ciprofloxacin and nalidixic acid resistance in tested
Salmonella Enteritidis isolates from Gallus gallus in reporting MSs, 20082014,
quantitative data
Table 17: Occurrence of resistance to selected antimicrobials in Salmonella spp. isolates from laying hens in 2014, using harmonised ECOFFs
Country Ampicillin Azithromycin Cefotaxime Ceftazidime Chloramphenicol Ciprofloxacin Colistin(a)
N % Res N % Res N % Res N % Res N % Res N % Res N % Res
Austria 45 6.7 45 0 45 0 45 0 45 2.2 45 8.9 45 17.8
Belgium 29 10.3 29 0 29 0 29 0 29 0 29 0 29 41.4
Croatia 19 0 19 0 19 0 19 0 19 0 19 15.8 19 0
Cyprus 17 11.8 17 0 17 0 17 0 17 0 17 35.3 17 0
France 86 7 86 0 86 1.2 86 1.2 86 2.3 86 0 86 15.1
Germany 80 13.8 80 1.3 80 0 80 0 80 0 80 7.5 80 10
Greece 43 4.7 43 0 43 0 43 0 43 0 43 14 43 0
Hungary 57 8.8 57 0 57 0 57 0 57 0 57 21.1 57 12.3
Italy 81 11.1 81 0 81 0 81 0 81 2.5 81 39.5 81 11.1
Poland 45 2.2 45 0 45 2.2 45 2.2 45 2.2 45 17.8 45 0
Portugal 38 7.9 38 0 38 0 38 0 38 5.3 38 18.4 38 13.2
Romania 46 23.9 46 2.2 46 2.2 46 2.2 46 0 46 43.5 46 8.7
Slovenia 15 0 15 0 15 0 15 0 15 0 15 0 15 0
Spain 138 8.7 138 0.7 138 0 138 0 138 2.2 138 15.2 138 8.7
United Kingdom 53 3.8 53 0 53 0 53 0 53 0 53 1.9 53 9.4
Total (MSs 15) 792 8.8 792 0.4 792 0.4 792 0.4 792 1.4 792 15.9 792 10.5
Croatia (N=11)
Czech Republic (N=8)
Denmark (N=1)
Italy (N=10) sus
Latvia (N=3) res1
Netherlands (N=25)
res2
Germany (N=20)
Greece (N=14) res3
Hungary (N=21) res4
Romania (N=15)
res5
Austria (N=7)
United Kingdom (N=7) res6
France (N=18) res7
Portugal (N=19)
res8
Poland (N=23)
Spain (N=20) res9
Belgium (N=14)
Estonia (N=1)
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 41: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Enteritidis from laying hens in MSs in 2014
Figure 42: Spatial distribution of ciprofloxacin resistance among Salmonella Enteritidis from laying
hens in countries reporting MIC data in 2014
Figure 43: Spatial distribution of nalidixic acid resistance among Salmonella Enteritidis from laying
hens in countries reporting MIC data in 2014
Figure 44: Spatial distribution of cefotaxime resistance among Salmonella Enteritidis from laying
hens in countries reporting MIC data in 2014
Resistance and multidrug resistance in S. Typhimurium isolates from laying hen flocks
Resistance levels to ampicillin, sulfamethoxazole and tetracycline (overall 18.826.6%) in
S. Typhimurium isolates from laying hens (Table TYPHILAYD) were found to be moderate to very
high levels. The overall resistance to chloramphenicol and trimethoprim was reported at low levels
(6.34.7%) whereas the resistance to the other antimicrobials tested required by the legislation was
not detected.
In laying hen flocks, 16.4% (18 MSs, N=67) of the S. Typhimurium isolates were multiresistant.
Microbiological co-resistance to ciprofloxacin and cefotaxime was not detected by any of the
reporting MSs (Tables COMTYPHILAY).
Resistance and multidrug resistance in monophasic S. Typhimurium isolates from laying hen flocks
Resistance levels to ampicillin, sulfamethoxazole and tetracycline (overall 37.587.5%) in
monophasic S. Typhimurium isolates from laying hens (Table MONTYPHILAYD) were observed at
very to extremely high levels. Resistance to chloramphenicol and trimethoprim was not reported,
whereas resistance to ciprofloxacin and nalidixic acid was registered only in one MS.
In laying hen flocks, 66.7% (three MSs, N=6) of the monophasic S. Typhimurium isolates were
multiresistant. Microbiological co-resistance to ciprofloxacin and cefotaxime was not detected by any
of the reporting MSs (Tables COMMONTYPHILAY).
Resistance and multi-drug resistance in S. Infantis isolates from laying hen flocks
The overall resistances in S. Infantis isolates from laying hens (14 MSs, Table 19), were much lower
than the one registered in broilers. Only 31.7% of the S. Infantis isolates from laying hens (13 MSs,
N=60) included in the MDR analysis were multiresistant (Figure 45, Tables COMINFANLAY).
Poland (N=6)
France (N=1)
Germany (N=1)
Spain (N=18)
sus
Greece (N=3) res1
Italy (N=3) res2
res3
Hungary (N=6) res4
Belgium (N=7) res5
res6
Austria (N=4) res7
Bulgaria (N=1) res8
res9
Croatia (N=2)
Cyprus (N=1)
Romania (N=7)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 45: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella Infantis from laying hens in MSs in 2014
Resistance and multidrug resistance in S. Infantis isolates from laying hen flocks
The overall resistances in S. Kentucky isolates from laying hens (five MSs, Table KENTLAYD), were
lower than those registered in broilers. 27.5% of the S. Kentucky isolates from laying hens (four MSs,
N=40) included in the MDR analysis were multiresistant (Figure 46, Tables COMINFANLAY).
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 46: Frequency distribution of completely susceptible isolates and resistant isolates to one to nine
antimicrobials classes in Salmonella Kentucky from laying hens in MSs in 2014
Table 18: Occurrence of resistance to selected antimicrobials in Salmonella Enteritidis isolates from laying hens in 2014
Country Ampicillin Azithromycin Cefotaxime Ceftazidime Chloramphenicol Ciprofloxacin Colistin(a)
N % Res N % Res N % Res N N % Res N % Res N % Res N
Austria 7 0 7 0 7 0 7 0 7 0 7 0 7 85.7
Belgium 14 0 14 0 14 0 14 0 14 0 14 0 14 85.7
Croatia 11 0 11 0 11 0 11 0 11 0 11 0 11 0
Czech Republic 8 0 8 0 8 0 8 0 8 0 8 0 8 50.0
Denmark 1 0 1 0 1 0 1 0 1 0 1 0 1 100
Estonia 1 0 1 0 1 0 1 0 1 0 1 100 1 0
France 18 16.7 18 0 18 0 18 0 18 5.6 18 0 18 16.7
Germany 20 0 20 0 20 0 20 0 20 0 20 0 20 35.0
Greece 14 7.1 14 0 14 0 14 0 14 0 14 0 14 0
Hungary 21 0 21 0 21 0 21 0 21 0 21 9.5 21 28.6
Italy 10 0 10 0 10 0 10 0 10 0 10 0 10 80.0
Latvia 1 0 1 0 1 0 1 0 1 0 1 0 1 100
Poland 23 4.3 23 0 23 4.3 23 4.3 23 0 23 34.8 23 0
Portugal 19 5.3 19 0 19 0 19 0 19 0 19 36.8 19 26.3
Romania 15 6.7 15 0 15 0 15 0 15 0 15 6.7 15 6.7
Spain 20 0 20 0 20 0 20 0 20 0 20 60 20 55.0
United Kingdom 7 0 7 0 7 0 7 0 7 0 7 14.3 7 28.6
Total (MSs 17) 210 3.3 210 0 210 0.5 210 0.5 210 0.5 210 15.2 210 31.9
Table 19: Occurrence of resistance to selected antimicrobials in Salmonella Infantis isolates from laying hens in 2014, using harmonised ECOFFs
Resistance levels in S. Derby and S. Kentucky isolates from fattening turkey flocks
High to extremely high levels of resistance to ampicillin, ciprofloxacin, gentamicin, nalidixic acid,
sulfamethoxazole and tetracycline were found in the S. Kentucky isolates included in the analysis
(six MSs, Table 20). In contrast, resistance to azithromycin, cefotaxime, ceftazidime, colistin and
trimethoprim was absent. In fattening turkeys, 69.1% of the S. Kentucky isolates (six MSs, N=55)
included in the MDR analysis were multiresistant and none of these isolates was found fully
susceptible (Tables COMKENTURK).
It is notable that isolates from Spain and the United Kingdom represented 96.9% of the S. Derby
isolates and the resistance to the antimicrobial tested varied remarkably between these two MSs
(Table 20). Spain reported MDR in all (145) S. Derby isolates (Tables COMDERBYTURK).
Table 20: Occurrence of resistance to selected antimicrobials in Salmonella spp., Salmonella Kentucky and Salmonella Derby isolates from turkeys in 2014
75
50
25
0
Germany Hungary Italy
% Resistant isolates
100
75
50
25
0
Poland Spain United Kingdom
100
75
50
25
0
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
Year
A statistically significant trend was observed for both ciprofloxacin and nalidixic acid in Austria (), France (), Italy (), Poland
(), Spain () and United Kingdom (), for ampicillin in Italy (), Poland (), Spain () and United Kingdom (), and Spain ().
Figure 47: Trends in ampicillin, cefotaxime, ciprofloxacin and nalidixic acid resistance in tested
Salmonella spp. isolates from turkeys in reporting MSs, 20082014, quantitative data
Figure 48: Spatial distribution of ciprofloxacin resistance among Salmonella spp. from fattening
turkeys in 2014
Figure 49: Spatial distribution of nalidixic acid resistance among Salmonella spp. from fattening
turkeys in 2014
Figure 50: Spatial distribution of cefotaxime resistance among Salmonella spp. from fattening
turkeys in 2014
Germany (N=13)
France (N=58)
sus
United Kingdom (N=162) res1
res2
Italy (N=35)
res3
Czech Republic (N=19) res4
res5
Poland (N=29)
res6
Austria (N=14) res7
res8
Hungary (N=170) res9
Spain (N=226)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
MS: Member State; N: total number of isolates tested for susceptibility against the whole common antimicrobial set for
Salmonella; sus: susceptible to all antimicrobial classes of the common set for Salmonella; res1res9: resistance to one
antimicrobial classes/resistance to nine antimicrobial classes of the common set for Salmonella.
Figure 51: Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from fattening turkeys in 2014
The term microbiological resistance is used when resistance is interpreted using the EUCAST
epidemiological cut-off values, whereas the term clinical resistance is noted when resistance is
analysed using the EUCAST clinical breakpoints.
Quinolone and fluoroquinolone resistance in the Enterobacteriaceae is mostly attributed to point
mutations in the quinolone resistance-determining regions (QRDR) of the gyrase ( gyrA and gyrB) and
topoisomerase IV (parC and parD) genes. Plasmid mediated quinolone resistance (PMQR) can be
caused by the the action of efflux pumps (qepA genes), enzymatic modifications (aac(6)-Ib-cr gene,
which also confers resistance to kanamycin), and protection of the DNA gyrase ( qnrA, qnrB, qnrD and
qnrS genes) (Cavaco et al., 2009).
The presence of two single point mutations in the QRDR will usually confer clinical resistance to
ciprofloxacin (minimum inhibitory concentration (MIC) > 0.064 mg/L) as well as to nalidixic acid
(MIC > 16mg/L). In contrast, isolates harbouring only one single point mutation in the QRDR will
usually show clinical resistance to nalidixic acid, whereas the susceptibility to ciprofloxacin is reduced
to only a microbiological resistance level.
In absence of other mechanisms, the presence of PMQR determinants (i.e. qnr genes) in a bacterium,
will confer only microbiological resistance to ciprofloxacin, but the isolate will be susceptible to
nalidixic acid.
Table 21: Occurrence of resistance to cefotaxime among Salmonella spp. from broilers, laying hens and fattening turkeys in 2014, using harmonised
ECOFFs and EUCAST CBPs
Salmonella spp.
The patterns of AMR exhibited by all reported Salmonella isolates revealed numerous combinations of
resistance to the nine different antimicrobial agents included in the analysis. The reported MSs
occurrence of specific MDR profiles in meat and animals are presented in the MDR patterns tables. In
broiler flocks, eight serovars (Infantis, Enteritidis, Mbandaka, Kentucky, Senftenberg, Typhimurium,
Agona and Montevideo) accounted for 74.1% of Salmonella spp. (Table SERBR). A further 102
serovars were reported from broilers and 44 of these were represented by only single isolates. In
laying hen flocks, eight serovars (Enteritidis, Typhimurium, Infantis, Kentucky, Montevideo,
Mbandaka, Senftenberg and Livingstone) accounted for 62.3% of Salmonella spp (Table SERLAY).
There were a further 75 serovars reported from laying hen flocks. In fattening turkey flocks, eight
serovars (Derby, Kentucky, Newport, Hadar, Infantis, Saintpaul, Bredeney and Stanley) accounted for
68.1% of Salmonella spp. (Table SEROFATTURK). There were a further 40 serovars reported from
fattening turkeys.
Detailed analysis of the specific patterns of resistance detected is most useful when performed at the
serovar level. However, the overall data from all Salmonella spp. have also been examined to
determine the pattern most common in highly prevalent sources per country. In broilers, where
982/2223 (44.2%) of isolates were MDR (Table MULTISALMBR) and broiler meat where 148/564
(26.2%) of isolates were MDR (Table MULTISALMBRMEAT), the most common resistance pattern was
a combination of ciprofloxacin/nalidixic acid, sulfamethoxazole and tetracycline, followed by the same
pattern with the addition of tigecycline, both patterns accounting for 22.4% of the broiler isolates and
19.2% of the broiler meat isolates included in the analysis. The majority of isolates with these
patterns of resistance both from broilers (95.8% of isolates with this pattern) and from broiler meat
(95.4% of isolates with this pattern) were S. Infantis. These resistant profiles were predominately
reported in broilers by Austria (98.2%), the Czech Republic (81.4%), Hungary (83.9%) and Slovakia
(84.6%) and in meat from broilers by Austria and the Czech Republic (100%), Hungary (89.2%),
Slovakia (77.8%) and Slovenia (92.9%). In laying hens the most common resistance pattern was the
same as in broilers: ciprofloxacin/nalidixic acid, sulfamethoxazole and tetracycline, followed by
ampicillin, ciprofloxacin/nalidixic acid and tetracycline (Table MULTISALMLAY). As in broilers, most of
the isolates (15/17, 88.2%) with resistance to ciprofloxacin/nalidixic acid, sulfamethoxazole and
tetracycline were S. Infantis.
In turkeys, where 432/726 (59.5%) of isolates were MDR, three serovars accounted for more than
50% of the MDR isolates, namely S. Derby (n=145 MDR isolates), S. Infantis (n=46 MDR isolates) and
S. Kentucky (n=38 MDR isolates). The most common patterns were related to single MSs such as the
most common pattern: ampicillin, ciprofloxacin/nalidixic acid, sulfamethoxazole, tetracycline and
trimethoprim being reported by Spain (representing 94.7% of total isolates reported with this
pattern). Most (92.6%) of the isolates with this MDR pattern were S. Derby. The second and third
most common patterns were mainly reported also by Spain: ampicillin, ciprofloxacin/nalidixic acid and
tetracycline (55.7%), and the MDR pattern ampicillin, chloramphenicol, ciprofloxacin/nalidixic acid,
sulfamethoxazole, tetracycline and trimethoprim (98.2%). In turkey meat, where 73/226 (32.3%) of
isolates were MDR, the two most common resistance patterns were ampicillin, chloramphenicol,
sulfamethoxazole, tetracycline, trimethoprim and ampicillin, ciprofloxacin/nalidixic acid, tetracycline,
each accounting for 17.8% of the total number of MDR isolates from turkey meat
(Table MULTISALMTURKMEAT).
Salmonella Enteritidis
Information on MDR was sparsely available for S. Enteritidis isolates and only reported from broilers
(16/74,21.6%) of isolates showed MDR and 16/305 (5.2%) of total S. Enteritidis isolates reported
from broilers, with MDR isolates originating from Poland, Portugal and Romania
(Table MULTIENTERBR) and laying hens (4/33,12.1%) of isolates showed MDR and 4/210 (1.9%) of
total S. Enteritidis isolates reported from laying hens, MDR isolates from France and Romania
(Table MULTIENTERLAY). One isolate from laying hens showed resistance to ampicillin,
chloramphenicol, sulfamethoxazole, tetracycline and trimethoprim. In broilers, 11/72 (15.3%) of
isolates were resistant to 5 or more antimicrobials, although MDR remains uncommon in S. Enteritidis
isolates. Most of the S. Enteritidis isolates from broilers (70.1%), broiler meat (64.0%) and laying
hens (77.1%) were fully susceptible to the 11 antimicrobials addressed in the analysis. A potentially
invasive clone of S. Enteritidis carrying virulence genes as well as MDR (Amp-Chl-Str-Sul-Tet-Tmp) has
been reported from the African continent and from travel-related cases in the United Kingdom
(Rodriquez et al., 2012). Streptomycin is however no longer included in the monitoring.
Salmonella Typhimurium
MDR S. Typhimurium isolates were reported in turkey meat (9 isolates were MDR out of 9
S. Typhimurium isolates reported) (Table MULTITYPHITURKMEAT), broilers (27 isolates were MDR out
of 87 S. Typhimurium isolates reported, 31.0%) (Table MULTITYPHIBR), laying hens (11 isolates were
MDR out of 64 S. Typhimurium isolates reported, 17.2%) (Table MULTITYPHILAY) and fattening
turkeys (9 isolates were MDR out of 21 S. Typhimurium isolates reported, 42.9%)
(Table MULTITYPHITURK). A wide range of different MDR patterns were reported in all sources. The
most frequent MDR pattern was resistance to ampicillin, sulfamethoxazole and tetracycline in most
sources. However, penta-, hexa- and hepta-valent resistance were reported in few isolate from
broilers and one from fattening turkeys. Resistance to cefotaxime/ceftazidime was reported with only
one isolate from broilers but was absent in all other sources. Ciprofloxacin resistance was not reported
in S. Typhimurium MDR isolates form laying hens.
Salmonella Kentucky
The patterns of MDR for S. Kentucky isolates were reported from meat from broilers (5 isolates were
MDR out of 33 isolates reported, 15.2%) (Table MULTIKENBRMEAT), meat from turkeys (4 isolates
were MDR out of 7 isolates reported, 57.1%) (Table MULTIKENTUCKYTURKMEAT), broilers (70
isolates were MDR out of 115 isolates reported, 60.9%) (Table MULTIKENTBR), laying hens (11
isolates were MDR out of 44 isolates reported, 25.0%) (Table MULTIKENTLAY) and fattening turkeys
(38 isolates were MDR out of 55 isolates reported, 69.1%) (Table MULTIKENTURK). About 55.7% of
the isolates from broilers had the core pattern of pentavalent resistance to ampicillin,
ciprofloxacin/nalidixic acid, gentamicin, sulfamethoxazole and tetracycline reported by the Cyprus, the
Czech Republic, Hungary, Romania and Spain. This core pentavalent resistance pattern was most
observed also in isolates in laying hens, fattening turkeys and turkey and broiler meat.
Salmonella Infantis
MDR patterns for S. Infantis were available from broiler meat (118 isolates were MDR out of 147
isolates reported, 80.3%) (Table MULTIINFANBRMEAT), turkey meat (7 isolates were MDR out of 9
isolates reported, 77.8%) (Table MULTIINFANBRMEAT), broilers (649 isolates were MDR out of 796
isolates reported, 81.5%) (Table MULTIINFANBR), laying hens (18 isolates were MDR out of 64
isolates reported, 28.1%) (Table MULTIINFANLAY) and fattening turkeys (46 isolates were MDR out of
53 isolates reported, 86.8%) (Table MULTIINFANTURK). In fattening turkeys most of the isolates
originated from Hungary (90.2%). S. Infantis displayed a wide range of different MDR patterns;
however, almost all MDR patterns (> 97%) included resistance to ciprofloxacin and/or nalidixic acid,
as well as resistance to sulfamethoxazole and tetracycline. Resistance to ciprofloxacin/nalidixic acid,
sulfamethoxazole and tetracycline was the most common pattern in S. Infantis from broiler meat
(74.6%), broilers (54.6%), laying hens (78.9%) and fattening turkeys (43.5%). All other
multiresistant S. Infantis isolates having resistance to cefotaxime and/or ceftazidime originated from
Cyprus (16.7%, n=3) and Italy broilers (60.0%, n=18).
3.1.3. Discussion
data on the other last-resort drugs, probably because the EU protocol for harmonised monitoring of
AMR in human Salmonella and Campylobacter isolates lists meropenem among the priority
antimicrobials and the others as optional (ECDC, 2014). In the absence of routine monitoring,
resistance to reserve agents may grow and remain undetected. Resistance to reserve agents that are
not used in food-producing animals may be related to cross-resistance to agents used in food-
producing animals for some agents, or to antimicrobial use in humans or exposure to sources of
Salmonella other than those associated with food-producing animals.
In terms of data quality and comparability, major improvements in harmonising data between
countries and across sectors have been made in the last two reports. In the data collection for the
2013 report, for the first time, countries could report measured values (quantitative AST data as
opposed to interpreted categories) to ECDC, and seven countries were then able to submit Salmonella
data in this way. For 2014, 12 countries were able to provide quantitative AST data, with four
countries changing from qualitative reporting and one country reporting AST data for the first time.
The quantitative data were interpreted based on EUCAST ECOFF values, where available. With respect
to categorical data, the categories of intermediate and resistant were combined in a non-
susceptible group. With this approach, the ECOFF-based category of wild type corresponds closely to
the susceptible category and the ECOFF-based category of non-wild type corresponds closely to the
non-susceptible category. Thus, this approach further improves the comparability of human and non-
human data. For countries submitting categorical data, only four were using other criteria than
EUCAST or did not communicate which criteria they were using. For future reports, EFSA and ECDC
hope that more countries will report measured values. More harmonisation is also needed when it
comes to the selection of isolates for testing and reporting at the EU level, as, in many countries, the
sampling and the antimicrobials tested for a particular selection are not random and represent
different fractions of all isolates identified in a country.
In 2014, some aspects of the reported human data remained difficult to interpret. For some countries,
the reported percentage of isolates resistant to ciprofloxacin was very low whereas the reported
percentage resistant to nalidixic acid was high. Whereas the proportion of isolates resistant to
fluoroquinolones might be expected to be slightly lower compared to quinolones, this difference was
considerable in some countries, and in two countries even as large as 20-fold and more than 100-fold.
Perhaps, some countries using disk diffusion (which applied to the majority of the human laboratories)
had not yet adopted the EUCAST recommendation, issued in early 2014, to screen for pefloxacin
susceptibility instead of ciprofloxacin in order to detect low-level fluoroquinolone resistance. It could
also be that some countries reporting interpreted results had not yet adapted to the new, significantly
lower CBP for ciprofloxacin, which was also introduced in 2014. The EU protocol will be updated on
these two points.
from turkeys. Considering all reporting MSs, isolates from laying hens displayed the lowest levels of
resistance to these antimicrobials. Levels of resistance were generally higher in S. Enteritidis from
broiler flocks than from laying hen flocks, particularly in the case of resistance to chloramphenicol,
tetracycline and sulfamethoxazole. This may reflect that laying hens are usually less frequently treated
with antimicrobials than broilers, although trimethoprim showed the reverse pattern. In many MSs,
only a limited number of antimicrobial compounds are authorised for the treatment of laying hens and
the relatively higher levels of ciprofloxacin resistance in layers may reflect that this is one of the
compounds available (although it is also available for the treatment of broilers) or may possibly reflect
an association of particular S. Enteritidis phage types which show low-level ciprofloxacin resistance
with laying hens.
Colistin-resistant Salmonella isolates were detected by several MSs originating from broilers, laying
hens and fattening turkeys. Further information is provided in the Summary/Main findings section.
The occurrence of resistance to fluoroquinolones (ciprofloxacin) was in general particularly related to
certain animal species and sources fattening turkeys, broilers, and meat thereof combined with a
clearly defined geographical distribution, including the following countries: Austria, Bulgaria, Croatia,
Cyprus, the Czech Republic, Hungary, Italy, Malta, Poland, Portugal, Romania, Slovenia, Slovakia and
Spain. In the reported data, it is clear that S. Kentucky and S. Infantis were mainly responsible for the
occurrence of fluoroquinolone resistance in the mentioned sources, which is highly suggestive of
clonal expansion (S. Kentucky ST198-X1) in the production of the food animals, especially poultry (Le
Hello et al., 2011, 2013b; Westrell et al., 2014). Although genetic typing of isolates would be required
for definitive confirmation, the predominance of particular MDR or other resistance patterns in isolates
of Infantis and Kentucky as well as published national reports also support clonal expansion.
Third-generation cephalosporins and fluoroquinolones are critically important for the treatment of
human salmonellosis. Co-resistance to cefotaxime and ciprofloxacin differed between MSs and was not
detected in isolates from the majority of MSs. In the single MS where it was detected (Spain), co-
resistance to these antimicrobials occurred in a single S. Kentucky isolate from broilers, which showed
high-level resistance to fluoroquinolones.
As in previous years, the reported levels of ciprofloxacin and nalidixic acid resistance in isolates from
the different types of meat or animal species between MSs were generally very similar; however,
isolates with resistance to ciprofloxacin, but susceptible to nalidixic acid, were also reported probably
indicating the occurrence of plasmid-mediated qnr genes leading to fluoroquinolone, but not nalidixic
acid, resistance. This was particularly a feature of Salmonella isolates from broilers in Malta, Portugal
and Spain and from turkeys in Hungary and Spain, although it was also present to a lesser extent in
isolates from layers from some MSs.
MDR, defined as resistance to three or more of eleven antimicrobial classes, was generally higher in
Salmonella spp. from broilers (46.3% of isolates) and turkeys (59.5% of isolates) than in layers (11%
of isolates). In broilers, the proportion of all isolates showing MDR, was greatly influenced by the
occurrence of MDR S. Infantis, this serovar accounting for approximately 31% of the MDR isolates in
broilers. Particular MDR patterns were associated with S. Infantis and because this serovar was
prevalent in many countries, these patterns greatly influenced the overall resistance figures. This is
exemplified by resistance to ciprofloxacin/nalidixic acid, sulfamethoxazole and tetracycline which
occurred as an MDR pattern without additional resistances in 355/762 (46.5%) of S. Infantis isolates;
Infantis represented 762/2,122 (35.9%) of all Salmonella isolates examined from broilers. Generally,
the resistance levels varied among serovars that may exhibit particular MDR patterns, so the relative
contribution of different serovars in different production types and between MSs should be kept in
mind when comparing the situation between the reporting countries.
The analysis of MDR resistance patterns also highlighted multiresistant strains of Salmonella occurring
in several MSs. High-level ciprofloxacin resistance (MIC > 4) was observed in multiresistant
S. Kentucky isolates from broilers, laying hens and turkeys, and in S. Infantis from broilers. It was
displayed by much lower numbers of other serovars (Enteritidis, Bonariensis, Kottbus) and was also
detected in S. Kentucky from broiler and turkey meat, and in S. Infantis from broiler meat. The MSs
reporting high levels of ciprofloxacin-resistant S. Kentucky and S. Infantis isolates in 2014 also
reported similar findings in 2013 (the Czech Republic, Hungary, Romania and Spain); however, more
MSs provided in 2014 isolate data suitable for the analysis of high-level ciprofloxacin resistance,
therefore more MSs found isolates with high-level resistance to ciprofloxacin. High-level ciprofloxacin
resistance is usually related to chromosomal mutations and therefore provides strong evidence for
clonal expansion of particular strains of Salmonella.
There were no Salmonella isolates recovered from poultry in 2014 which were resistant to
carbapenems, a class of antimicrobials which is not used therapeutically in food-producing animals,
but which is reserved for use in man. Supplementary testing of those Salmonella isolates which were
resistant to the indicator cephalosporins (cefotaxime and ceftazidime) with a further panel of
antimicrobials revealed the presence of isolates with ESBL, AmpC and combined ESBL plus AmpC
phenotypes. Most MSs reported low numbers of isolates with these phenotypes, though in two MSs,
two serovars (Infantis with an ESBL phenotype in Italy; Heidelberg with an ampC phenotype in the
Netherlands) contributed to moderate or high levels of cephalosporin resistance in Salmonella from
broilers. The occurrence of S. Infantis with an ESBL phenotype and S. Heidelberg with an AmpC
phenotype in restricted geographical regions of Europe suggests clonal expansion and spread within
broilers in these regions.
Within a given MS, any attempt to relate AMR in human Salmonella isolates to AMR in isolates from
food and food-producing animals in that MS is complicated, because much of the food consumed in an
MS may have originated in other MSs or in third countries. Salmonella infections can also be
associated with foreign travel, other types of animal contact (such as pet reptiles) or the environment.
Some human infections can also occur through spread between affected human patients. To improve
investigation of these relationships, isolates from cases notified as having been acquired during travel
outside of the reporting country were excluded from the analysis, except with respect to the analysis
of resistance in different geographical regions. The comparison would further improve if a distinction
could be made between food isolates from domestically produced animals and those from other
countries, although this is not currently possible.
In 2014, 13 MSs and Norway provided data on human Campylobacter isolates for 2014. Eight
countries (Austria, Estonia, Italy, Luxembourg, Norway, Portugal, Romania and Slovenia) reported
quantitative isolate-based AST results as measured values of either inhibition zone diameters or MICs.
Six countries reported case-based AST results interpreted as susceptible (S), intermediate (I) or
resistant (R) according to the CBPs applied. Countries reporting resistance in Campylobacter from
humans in 2014 are presented in Tables CAMPJEOVERVIEW and CAMPCOOVERVIEW. The report only
addressed data on C. jejuni and C. coli for comparison with AST data on food-producing animals and
food, and as these Campylobacter species are the most commonly identified cause of
campylobacteriosis in humans in the EU. Quantitative isolate-based data on AMR in Campylobacter
isolates from poultry and meat derived thereof were reported by 26 MSs and two non-MSs Iceland
and Switzerland. AST was carried out for C. jejuni and C. coli only; all other Campylobacter species
were excluded from the monitoring programme of antimicrobial resistance in Campylobacter (Tables
CAMPJEOVERVIEW and CAMPCOOVERVIEW).
Figure 53: Comparison of CBPs and ECOFFs used to interpret MIC data reported for
Campylobacter spp. from humans, animals or food
Table 22: Antimicrobial resistance in Campylobacter jejuni from humans per country in 2014
Figure 54: Frequency distribution of Campylobacter jejuni isolates from humans completely
susceptible or resistant to one to four antimicrobial classes in 2014
Spatial distribution of resistance among Campylobacter jejuni isolates from human cases
The spatial distribution of ciprofloxacin resistance in C. jejuni isolates from human cases (Figure 55)
shows that the highest proportion of resistance was reported by southern European and Baltic
countries, whereas northern and central European countries reported lower levels. Erythromycin
resistance levels were higher in the southern European countries and in Norway (Figure 56).
Figure 55: Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from human
cases in reporting countries in 2014
Figure 56: Spatial distribution of erythromycin resistance among Campylobacter jejuni from human
cases in reporting countries in 2014
Table 23: Antimicrobial resistance in Campylobacter coli from humans per country in 2014
Figure 57: Frequency distribution of Campylobacter coli isolates from humans completely susceptible
or resistant to one to four antimicrobial classes in 2014
Resistance levels among C. jejuni and C. coli isolates from meat from broilers
For 2014, four MSs provided antimicrobial resistance data on C. jejuni and C. coli isolates from broiler
meat (Table 24). Although resistance is typically higher among C. coli than C. jejuni isolates, common
features in the levels of resistance to ciprofloxacin, erythromycin, gentamicin, nalidixic acid and
tetracyclines can be observed in the two Campylobacter species monitored. Resistance to tetracyclines
and nalidixic acid generally ranged from high to extremely high levels, whereas resistance to
gentamicin varied less among reporting MSs and was either undetected or recorded at very low level
(0.6%). For those antimicrobials of particular importance in treating human Campylobacter infections,
resistance to ciprofloxacin was in general very high to extremely high in reporting MSs and, as
expected, closely paralleled the results obtained for nalidixic acid, whereas resistance to erythromycin
was much lower considering all reporting MSs. In contrast to the other two reporting MSs, Denmark
recorded a moderate resistance level (15.4%) to ciprofloxacin and nalidixic acid in C. jejuni, although
a low number of isolates was tested. The recorded levels of resistance to erythromycin considering
C. jejuni and C. coli were contrasting, with higher resistance observed in C. coli.
MDR among C. jejuni and C. coli isolates from meat from broilers
The isolate-based resistance data on 10 or more isolates of C. jejuni and C. coli were not available
from broiler meat; the corresponding MDR analysis is not presented in this report.
Table 24: Occurrence of resistance to selected antimicrobials in Campylobacter coli and Campylobacter jejuni from meat in 2014, using harmonised ECOFFs
Representative monitoring
In 2014, the implementation of Commission Implementing Decision 2013/652/EU, which sets out the
requirements for monitoring resistance in C. jejuni in broilers, resulted in comprehensive monitoring in
25 MSs and one non-MS (Iceland) on C. jejuni and C. coli isolates from broilers (Table 25). On a
voluntary basis, eight MSs also monitored resistance in C. coli in broilers. Further information on the
representative sampling of carcases of healthy broilers at the slaughterhouse may be found in the
Material and methods section.
Table 25: Occurrence of resistance to selected antimicrobials in Campylobacter from broilers in 2014, using harmonised ECOFFs
75
50
25
0
France Germany Hungary Netherlands
% Resistant isolates
100
75
50
25
0
Slovenia Spain Sweden Switzerland
100
75
50
25
0
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
Year
Figure 58: Trends in ciprofloxacin, erythromycin and nalidixic acid resistance in Campylobacter jejuni
from broilers in MSs, 20082014
75
50
25
% Resistant isolates
75
50
25
0
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
Year
Figure 59: Trends in ciprofloxacin, erythromycin and nalidixic acid resistance in Campylobacter coli
from broilers in MSs, 20082014
Figure 60: Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from broilers
of Gallus gallus in reporting countries in 2014
Figure 61: Spatial distribution of erythromycin resistance among Campylobacter jejuni from broilers
of Gallus gallus in reporting countries in 2014
Multidrug resistance among Campylobacter jejuni and Campylobacter coli isolates from broilers
A large variation in the levels of complete susceptibility to the common set of antimicrobials for
Campylobacter (four antimicrobials) was observed among the reporting countries. Complete
susceptibility was generally found in more than 10.0% of the C. jejuni isolates tested in the reporting
MSs, and reached up to 91.2% in Sweden and 96.4% in Iceland, whereas in Bulgaria, Cyprus, Greece,
Hungary, Italy, Poland, Portugal and Spain, the proportion of fully susceptible isolates was much lower
(under 10.0%). The overall complete susceptibility of the C. jejuni isolates was assessed at 23.1%.
MDR in C. jejuni isolates was recorded in 11 countries (out of 26 reporting data), generally at low
levels, although, in Bulgaria, 29.1% of isolates exhibited MDR. The overall MDR of the C. jejuni
isolates was 4.6% (Table COMCAMPJEBR).
The important co-resistance15 for public health to both ciprofloxacin and erythromycin in C. jejuni was
detected in 14 out of 26 reporting countries, with Bulgaria reporting the highest occurrence of co-
resistance in 34.5% of isolates. The overall co-resistance to ciprofloxacin and erythromycin in C. jejuni
was 4.8% for all reporting MSs.
In C. coli, complete susceptibility was generally lower (18.3%) than that observed in C. jejuni and the
occurrence of MDR was greater (18.3%) than that reported in C. jejuni isolates
(Table COMCAMPCOBR). In C. coli isolates, co-resistance to ciprofloxacin and erythromycin was
detected in six out of nine MSs, with Spain reporting the highest occurrence in 33.3% of isolates;
resulting in an overall co-resistance in C. coli of 18.3%.
The frequency distributions of the numbers of antimicrobials to which individual isolates were resistant
(Figure 62 and Figure 63) showed marked variation between different reporting countries. Although
most of the reporting countries detected resistance to a maximum of two antimicrobial classes in
C. jejuni, Portugal, Romania and Bulgaria reported MDR levels ranging between 10 and nearly 30%
(Figure 62). Conversely, in reporting MSs, C. coli isolates displayed more frequently resistance to three
different classes of antimicrobials (Figure 63), notably in Germany and Spain where the occurrence of
MDR exceeded 20% .
Patterns of multidrug resistance in Campylobacter jejuni and Campylobacter coli isolates from broilers
Considering C. jejuni, isolate-based data were available from 25 contributing MSs and one non-MS,
which in total reported details of 3,345 isolates. The isolates reported by 14 MSs (44.5% from the
total number of the isolates reported) and Iceland are not addressed in the Table MULTICAMPJEGBR,
as they were not multiresistant. Considering C. coli, analysis of the patterns of resistance to
erythromycin, ciprofloxacin/nalidixic acid, tetracyclines and gentamicin was possible for 622 C. coli
isolates from six contributing MSs (Table MULTICAMPCOBR).
Among the 1,842 C. jejuni isolates from broilers from the reporting MSs submitting isolates which
were multiresistant, 8.4% (n=155) exhibited MDR (Table MULTICAMPJEGBR). The most common
pattern of MDR was resistance to ciprofloxacin/nalidixic acid, erythromycin and tetracyclines, occurring
in 135 out of 155 resistant isolates (and constituting the core resistance pattern in a further 13
isolates, which also showed gentamicin resistance) reported by submitting MSs. The situation
regarding the patterns was similar in C. coli (Table MULTICAMPCOBR), but with a higher percentage
(16.9%) of the isolate displayed MDR of all isolates were available (N=622). Gentamicin resistance, as
a component of MDR patterns in C. coli, was observed only in Romania and Spain. Romania
contributed isolates with a greater range of different resistance patterns than other MSs, although this
may have merely reflected the small isolate sample size from other MSs.
15
The term co-resistance has been defined as two or more resistance genes which are genetically linked, i.e. located adjacent
or close to each other on a mobile genetic element (Chapman, 2003). For brevity, the term is used slightly more loosely in
this report and indicates two or more phenotypic resistances to different classes of antimicrobials, exhibited by the same
bacterial isolate.
Iceland (N=28)
Sweden (N=102)
Denmark (N=165)
Finland (N=88)
Ireland (N=99)
Croatia (N=65)
United Kingdom (N=165)
Belgium (N=92)
Slovakia (N=11)
Netherlands (N=98)
Germany (N=195) sus
Austria (N=193)
res1
Czech Republic (N=47)
France (N=175) res2
Slovenia (N=77) res3
Lithuania (N=37)
res4
Romania (N=447)
Cyprus (N=69)
Italy (N=261)
Hungary (N=150)
Bulgaria (N=110)
Greece (N=80)
Poland (N=179)
Portugal (N=240)
Spain (N=80)
Latvia (N=92)
Figure 62: Frequency distribution of Campylobacter jejuni isolates completely susceptible and
resistant to one to four antimicrobials, in broilers in MSs, 2014
Croatia (N=92)
Netherlands (N=39)
Slovenia (N=30)
sus
Romania (N=316) res1
res2
Slovakia (N=36)
res3
res4
Germany (N=111)
Czech Republic
(N=52)
Spain (N=90)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Figure 63: Frequency distribution of Campylobacter coli isolates completely susceptible and resistant
to one to four antimicrobials, in broilers in MSs, 2014
Representative monitoring
For 2014, resistance data on Campylobacter isolates from fattening turkeys (Table 26) were provided
by 10 MSs. Commission Implementing Decision 2013/652/EU lays down that monitoring resistance in
C. jejuni in fattening turkeys is mandatory in those MSs where the production of turkey meat is
greater than 10,000 tonnes slaughtered per year. Three MSs also reported data on C. coli in fattening
turkeys. Further information on the representative sampling of carcases of healthy broilers at the
slaughterhouse may be found in the Material and methods section.
Temporal trends in resistance among Campylobacter jejuni from fattening turkeys isolates
None of MSs provided resistance data for C. jejuni from fattening turkeys isolates on 5 years or more
to be included in the statistical analysis.
Spatial distribution of resistance among Campylobacter jejuni isolates from fattening turkeys
The spatial distributions of ciprofloxacin and erythromycin resistance in C. jejuni isolates from
fattening turkeys (Figure 64 and Figure 65) show that the highest levels of resistance to these
substances were reported by southern European countries, whereas northern European countries
reported lower levels.
Table 26: Occurrence of resistance to selected antimicrobials in Campylobacter from fattening turkeys in 2014, using harmonised ECOFFs
Figure 64: Spatial distribution of ciprofloxacin resistance among Campylobacter jejuni from fattening
turkeys in reporting countries in 2014
Figure 65: Spatial distribution of erythromycin resistance among Campylobacter jejuni from
fattening turkeys in reporting countries in 2014
Austria (N=73)
United Kingdom
(N=152)
Germany (N=187)
France (N=174)
sus
Poland (N=171) res1
res2
Italy (N=153)
res3
Romania (N=14) res4
Hungary (N=87)
Portugal (N=72)
Spain (N=37)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Figure 66: Frequency distribution of Campylobacter jejuni isolates completely susceptible and
resistant to one to four antimicrobials, in fattening turkeys in MSs, 2014
3.2.3. Discussion
16
A representative of the macrolides commonly used in the treatment of human campylobacteriosis.
17
A representative of the fluoroquinolones commonly used in the treatment of human campylobacteriosis.
countries, whereas northern and central European countries reported lower levels. A similar spatial
distribution was observed in isolates from broilers.
Given the corresponding data on isolates of food or animal origin, with particularly high levels of
resistance to fluoroquinolones in broilers, and the understanding that a large proportion of human
campylobacteriosis infections comes from handling, preparing and consuming broiler meat or can be
attributed to the chicken reservoir as a whole (EFSA BIOHAZ Panel, 2010a), this is a compelling
example of the impact of acquired antimicrobial resistance in food and animals on the availability of
effective antimicrobial agents for treating some zoonotic human infections.
Human antimicrobial susceptibility data were available for all antimicrobials included in the MDR
analysis from five MSs and Norway for C. jejuni and from four MSs for C. coli. Overall, only one in five
human C. jejuni isolates and one in six human C. coli isolates were fully susceptible to all tested
antimicrobials. Multi-drug resistance18 was low (0.4%) in C. jejuni but significantly higher (10.4%) in
C. coli with two of four countries reporting MDR in about half of the isolates (though the number of
tested isolates were low). It is important to emphasise that all antimicrobials included in the MDR
analysis since the 2013 report are of clinical relevance. Clinical and microbiological co-resistance to the
critically important antimicrobials ciprofloxacin and erythromycin was low in C. jejuni but moderate in
C. coli with two countries reporting high to very high co-resistance levels to the two primary agents
used for treatment.
In terms of data quality and comparability, major improvements in harmonising data between
countries and across sectors have been made during the last two data collections. In the data
collection for the 2013 report, for the first time, countries could report measured values (quantitative
AST data as opposed to interpreted categories) to ECDC and five countries did so. For 2014, eight
countries provided quantitative AST data, with three countries changing from qualitative reporting,
one country reporting AST data for the first time and one country that did not report, compared to
2013. The quantitative data were interpreted based on EUCAST ECOFF values, where available. With
respect to categorical data, the categories of intermediate and resistant were combined in a non-
susceptible group. With this approach, the ECOFF-based category of wild type corresponds fully to
the susceptible category and the ECOFF-based category of non-wild type corresponds closely to the
non-susceptible category with only one exception for tetracyclines and C. jejuni. Thus, this approach
further improves the comparability of human and non-human data. Of countries submitting categorical
data, all but one was using EUCAST criteria in 2014, a significant stride towards harmonisation
compared with 2012. For future reports, EFSA and ECDC hope that more countries will report
measured values. More harmonisation is also needed when it comes to the sampling of isolates for
testing and reporting at the EU level, as, in many countries, the sampling and the antimicrobials
tested for a particular sample are not random, and represent different fractions of all isolates
identified in a country.
As in the two previous reports, isolates from cases notified as having been acquired while travelling
abroad were excluded from the analysis. The rationale is to facilitate assessment of the relationship
between antimicrobial resistance in Campylobacter isolates from food and food-producing animals
with antimicrobial resistance in human isolates of Campylobacter spp. As imported or traded food can
constitute a large proportion of the food available in some countries, the relationship between
resistance in food and food-producing animals and in the human population remains complex.
18
MDR is defined as microbiological resistance to at least three of the four different antimicrobial classes tested.
Overall, the levels of antimicrobial resistance in Campylobacter isolates from food in 2014 were higher
than those observed in 2013, although fewer countries reported data in 2014, comparing with 2013.
Because of the marked differences in the levels of resistance observed between some countries,
variation in those countries which report data each year can add to the variability observed in overall
figures for all reporting MSs. The monitoring of antimicrobial resistance in C. jejuni isolates from
broilers was mandatory in 2014 and therefore, the majority of the MSs (25) reported data, compared
with 2013, when only 11 MSs reported data. Levels of resistance in C. jejuni isolates from broilers
were higher than those observed in 2013.
The resistance exhibited by C. jejuni and C. coli isolates to ciprofloxacin and tetracyclines varied very
widely between MSs; in the case of C. jejuni and erythromycin, resistance levels were generally low or
resistance was not detected, whereas, for C. coli, there was again a wide variation in levels or
resistance at the MS level, irrespective of the source of the isolates.
In 2014, ciprofloxacin resistance in C. jejuni isolates from humans was 60.2% for all contributing MSs
(range: 50.647.9%), 69.8% in broilers (range: 3.9100%) and 69.6% in fattening turkeys (range:
34.695.4%). The picture is clearly complex in relation to the sources of human infections because
these may be related to consumption of broilers or turkeys meat (as well as other sources).
International trade also means that consumers may be exposed to meat produced in a number of
different countries. Despite the fact that imported food can contribute to cases of Campylobacter
infection, there were striking parallels in the observed occurrence of resistance to ciprofloxacin,
erythromycin, gentamicin and tetracyclines in C. jejuni isolates from broiler meat, broilers and man in
Austria, and in C. coli isolates from broiler meat and man in Portugal, with similar levels of resistance
to each antimicrobial seen in isolates originating from these different sources within each country.
Austria and Portugal were the only MSs which reported results for Campylobacter isolates from meat
and from human cases of infection. Interestingly, Austria also reported results for C. jejuni from meat
from turkeys and fattening turkeys; isolates from turkeys also closely paralleled the results obtained
for isolates from human cases, whereas ciprofloxacin resistance was rather higher in isolates from
turkey meat. From 2008 to 2014, statistically significant increasing trends in ciprofloxacin and nalidixic
acid resistance in C. jejuni from broilers were observed over 5 or more years in six reporting
countries; this was also observed in C. coli from broilers in two reporting countries.
Regarding resistance to erythromycin in all reporting MSs, erythromycin resistance in C. jejuni from
broilers and fattening turkeys was 5.9% and 0.7%, respectively, whereas, in C. coli resistance was
14.5% and 43.3%, respectively. Erythromycin resistance showed increasing trends in C. coli from
broilers in two countries, whereas erythromycin resistance showed a decreasing trend in C. jejuni
from broilers in four countries. The range of dilutions over which erythromycin is currently tested is
limited and thus, an analysis of resistance at much higher levels was not possible from the current
data. Particular resistance mutations have been associated with high-level erythromycin resistance
and further evaluation of the resistance detected to erythromycin could include such an evaluation.
This might be particularly relevant where resistance is already high, as a possible indication of on-
going high selective pressure. Recently, transferable macrolide resistance has been detected and this
confers high level macrolide resistance (further information is presented in the text box below).
Campylobacter can develop resistance to several of the different antimicrobials in the common test
panel by different mechanisms. Resistance to ciprofloxacin and erythromycin in Campylobacter is
usually the result of mutation with or without the additional action of efflux pumps (Piddock et al.,
2003; Ge et al., 2005; Luangtongkum et al., 2009). The efflux pump CmeABC acting alone has also
been shown to confer a degree of resistance to erythromycin, ciprofloxacin and tetracyclines (Ge et
al., 2005). Tetracycline resistance, which can therefore be related to CmeABC, was commonly shown
in a British study to be related to the presence of the tetracycline resistance gene tet(O) (Piddock et
al., 2008), which encodes a protein promoting the release of tetracycline from its binding site (Connell
et al., 2003). The existence of different resistance mechanisms conferring either resistance against the
different individual compounds or resistance against combinations of compounds complicates the
process of trying to infer the genotype from the phenotype and account for the multiple resistance
patterns detected. Isolates of both C. coli and C. jejuni, from animals and humans19, showed
resistance to erythromycin, ciprofloxacin and tetracyclines, raising the possibility that CmeABC may
19
Of the human Campylobacter isolates in 2014, 42 C. jejuni and 48 C. coli isolates were resistant to all these three substances
(data not shown in the section).
have been responsible for or contributed to the observed pattern of resistance. Only 14/3,317 (0.4%)
of C. jejuni, 10/767 (1.3%) of C. coli from broilers and 1/1,121 (0.09%) of C. jejuni from turkeys were
resistant to the combination erythromycin, ciprofloxacin and tetracyclines, without showing nalidixic
acid resistance. CmeABC may also have contributed to the MDR patterns of resistance shown by
isolates which were resistant to erythromycin, ciprofloxacin, nalidixic acid and tetracyclines, but in
which gyrA mutations were also present conferring both ciprofloxacin and nalidixic acid resistance.
The frequently high levels of tetracycline resistance observed in Campylobacter may in part be a
consequence of the presence of the tetracycline resistance gene tet(O) on a transferable plasmid
facilitating dissemination of tetracycline resistance (Wieczorek and Osek, 2013), although tet(O) may
also be chromosomally located in Campylobacter (Piddock et al., 2008). Recently, a transferable
plasmid bearing the macrolide resistance gene erm(B) which confers high-level macrolide resistance,
has been described (Wang et al. 2014). This is an important development, because macrolide
resistance up to this point appears to have been mutational rather than related to transferable,
plasmid-mediated resistance mechanisms in Campylobacter and the occurrence of plasmid-mediated
resistance may allow the much wider dissemination of macrolide resistance than has previously been
observed. AS the erm(B) gene confers erythromycin MICs of 512 mg/L, it may be necessary in the
future to review the dilution range of erythromycin which is tested. In 2014, 75/3,504 (2.1%) C. jejuni
and 71/795 (8.9%) C. coli isolates from broilers, as well as 11/1,123 (1.0%) C. jejuni and 134/390
(34.4%) C. coli isolates from turkeys had MICs of >128mg/L (the highest dilution tested), so if erm(B)
is present in these Campylobacter isolates, from the current monitoring, an upper ceiling can be
placed on the proportion of the total number of isolates which might carry this gene.
Gentamicin resistance in Campylobacter was uncommon in broilers and fattening turkeys isolates, but
where it did occur in multiple-resistant isolates of C. coli and C. jejuni, streptomycin resistance was
usually also observed in previous years. Streptomycin is now tested on a voluntary basis and was not
included in the MDR analysis for 2014. Recently a cluster of aminoglycoside-modifying enzymes has
been reported in C. coli from broiler chickens in China (Qin et al., 2012). An increase in gentamicin
resistance in C. coli from retail chicken the USA has recently been observed (FDA, 2011), with most
isolates originating from the western region of the USA and apparently related to the clonal expansion
of a particular C. coli lineage. The resistance gene aph(2)-Ig was responsible for conferring
gentamicin resistance in these USA retail chicken C. coli isolates and was colocated on a plasmid
which also carried tet(O) resistance (Zhao et al., 2015). Gentamicin resistance was detected in
C. jejuni from broilers and turkeys, and C. coli from broilers in EU MSs in 2014, although whether
clonal expansion of strains is also playing any role in the occurrence of gentamicin resistance in these
Campylobacter isolates is not known.
The molecular basis for the observed patterns of MDR was not reported for the isolates, but molecular
investigation and characterisation of selected isolates, representative of particular patterns of
importance or interest, would assist greatly in determining significance and assessing the potential for
further dissemination through, for example, co-selection or the occurrence of conjugative plasmids.
Figure 67: Erythromycin resistance in C. jejuni and C. coli from broilers and fattening turkeys
Rationale for monitoring AMR in indicator E. coli in food-producing animals and food
Commensal E. coli is typically chosen as an indicator of antimicrobial resistance in Gram-negative
bacteria, as it is commonly present in animal faeces, may be relevant to human medicine and can
often acquire conjugative plasmids, which are resistance determinants transferred between enteric
bacteria. Commensal E. coli, present in the intestines of food-producing animals, can constitute a
reservoir of resistance genes that can spread horizontally to zoonotic and other bacteria present in the
food chain. The monitoring of antimicrobial resistance in indicator E. coli, isolated from either
randomly selected healthy animals or carcases and meat derived thereof, and chosen to be
representative of the general population, provides valuable data on the resistance occurring in that
population. Determining the occurrence of resistance to antimicrobials in indicator E. coli provides
data useful for investigating the relationship with the selective pressure exerted by the use of
antimicrobials on the intestinal population of bacteria in food-producing animals. Indicator E. coli is
also helpful as representative of the Enterobacteriaceae to monitor the emergence and changes in the
proportion of bacteria producing ESBLs. Since 2014, the mandatory monitoring of AMR in indicator
E. coli from food-producing animals and food thereof has laid down inthe EU legislation.
In total, 27 MSs and two non-MSs reported quantitative MIC data in commensal (indicator) E. coli
isolates from poultry populations in 2014 (Table ESCHEOVERVIEW). Two of these countries provided
MIC data on isolates collected from poultry meat. Antimicrobial susceptibility data were interpreted
using ECOFFs laid down in Commission implementing Decision 2013/652/EC to determine organisms
exhibiting reduced susceptibility, i.e. showing microbiological resistance (as opposed to clinical
resistance).20
For further information on antimicrobials tested by the reporting countries and the reported MIC
distributions for E. coli in 2014, please refer to Table 5 and Table 7 in the Material and methods
chapter and to the submitted and validated MS data published on the EFSA website, respectively.
20
Of particular note is that microbiological resistance to ciprofloxacin was addressed using ECOFF CIP >0.064 mg/L in this
report (see Section 3.3.5 Discussion, for further details).
Table 27: Occurrence of resistance to selected antimicrobials in indicator Escherichia coli from broilers in MSs reporting data in 2014
Temporal trends in resistance among indicator Escherichia coli isolates from broilers
Temporal trends in resistance to selected antimicrobials in indicator E. coli isolates from broilers over
the 7-year study period from 2008 to 2014 are displayed on Figure 68 and Figure 69. Four MSs and
Switzerland provided resistance data on 5 years or more to be included in the statistical analysis.
Marked discrepancies in resistance levels between reporting MSs was observed for many of the
antimicrobials. France, Spain and the Netherlands tended to report the highest levels of resistance to
most antimicrobials over the period, although Austria, Spain and the Netherlands recorded the highest
resistance to quinolones between 2010 and 2014, and France, Spain and the Netherlands registered
the highest resistance to tetracyclines from 2008 to 2014. Conversely, Denmark generally recorded
the lowest resistance levels reported.
The resistance to ciprofloxacin reported over the study period was high to very high for all reporting
countries, with the exception of Denmark for the whole period. A close similarity in resistance levels to
ciprofloxacin and nalidixic acid was observed in most MSs. Such inter-annual evolutions need to be
confirmed by longer term trends.
Although resistance to many of the antimicrobials was broadly stable or had shown only gradual
increases or decreases over the study period, statistically significant trends in resistance to some of
the antimicrobials over 5 or more years were discerned. France and Switzerland recorded significant
increases in resistance to ampicillin, ciprofloxacin and nalidixic acid, and cefotaxime only by France,
while, contrastingly, the Netherlands reported significant declines in resistance to ampicillin,
cefotaxime, ciprofloxacin, nalidixic acid and tetracyclines over the last 5 years.
Figure 68: Trends in ampicillin and tetracyclines resistance in indicator Escherichia coli from broilers
in reporting countries, 20082014
75
50
25
0
Germany Netherlands Poland
% Resistant isolates
100
75
50
25
0
Spain Switzerland
100
75
50
25
0
2008
2009
2010
2011
2012
2013
2014
2008
2009
2010
2011
2012
2013
2014
Year
Figure 69: Trends in cefotaxime, ciprofloxacin and nalidixic acid resistance in indicator
Escherichia coli from broilers in reporting countries, 20082014
Figure 70: Spatial distribution of ciprofloxacin resistance among indicator Escherichia coli from
broilers in reporting countries, in 2014
Figure 71: Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from
broilers in reporting countries, in 2014
Figure 72: Spatial distribution of cefotaxime resistance among indicator Escherichia coli from broilers
in reporting countries, in 2014
Norway (N=205)
Finland (N=175)
Sweden (N=197)
Denmark (N=191)
Austria (N=176)
Germany (N=227)
Netherlands (N=377) sus
Czech Republic (N=196) res1
Ireland (N=167) res2
France (N=226)
res3
United Kingdom (N=159)
Hungary (N=170) res4
Cyprus (N=87) res5
Belgium (N=158) res6
Slovenia (N=85)
res7
Spain (N=170)
Italy (N=170) res8
Croatia (N=170) res9
Latvia (N=143)
Poland (N=179)
Estonia (N=71)
Portugal (N=201)
Greece (N=172)
Slovakia (N=85)
Lithuania (N=81)
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Figure 73: Frequency distribution of Escherichia coli isolates completely susceptible and resistant to
one to twelve antimicrobials in broilers in reporting countries, 2014
Resistant to
Resistant to both
MDR patterns of isolates resistant to both CIP both CIP and
CIP and CTX,
Country N and CTX CTX, applying
applying ECOFFs
(number of isolates) CBPs
N % Res N % Res
Austria 176 CTX-CAZ-CIP-AMP-NAL(1) 1 0.6
Belgium 158 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET(2) 13 8.2 4 2.5
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CAZ-CIP-AMP-NAL(1)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2)
CTX-CAZ-CIP-AMP-NAL-SMX-TMP(3)
CTX-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CIP-AMP-NAL-SMX-TMP(1)
Resistant to
Resistant to both
MDR patterns of isolates resistant to both CIP both CIP and
CIP and CTX,
Country N and CTX CTX, applying
applying ECOFFs
(number of isolates) CBPs
N % Res N % Res
GEN-CHL-CTX-CAZ-CIP-AMP-NAL(1)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
Croatia 170 GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1) 1 0.6
Cyprus 87 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2) 28 32.2 18 20.7
CTX-CAZ-CIP-AMP-NAL(4)
CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(11)
CTX-CAZ-CIP-AMP-NAL-TET(1)
CTX-CAZ-CIP-AMP-NAL-TET-TMP(1)
CTX-CIP-AMP-NAL-SMX-TET-TMP(2)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(4)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2)
Czech 196 CTX-CAZ-CIP-AMP-NAL(2) 2 1.0
Republic
Estonia 71 CTX-CAZ-CIP-AMP-NAL(2) 3 4.2
CTX-CIP-AMP-NAL(1)
France 226 CTX-CAZ-CIP-AMP-NAL-SMX-TET(3) 4 1.8
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
Germany 227 CHL-CTX-CAZ-CIP-AMP-COL-NAL-SMX-TMP(1) 2 0.9
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
Greece 172 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1) 4 2.3 4 2.3
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TMP(1)
GEN-CHL-CTX-CAZ-CIP-AMP-SMX-TET-TMP(1)
Hungary 170 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1) 4 2.4 1 0.6
CTX-CAZ-CIP-AMP-NAL(3)
Ireland 167 CTX-CAZ-CIP-AMP-NAL-SMX-TET(1) 2 1.2
CTX-CIP-AMP-NAL-SMX-TET(1)
Italy 170 CHL-CTX-CAZ-CIP-AMP-COL-NAL-SMX-TET-TMP(1) 5 2.9 2 1.2
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CIP-AMP-NAL-SMX-TET-TMP(1)
GEN-CHL-CTX-CAZ-CIP-AMP-SMX-TET(1)
Latvia 143 CHL-CTX-CAZ-CIP-AMP-NAL-SMX(4) 43 30.1 15 10.5
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET(4)
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(18)
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TMP(4)
CHL-CTX-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CAZ-CIP-AMP-NAL(3)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(3)
CTX-CAZ-CIP-AMP-NAL-TET(1)
CTX-CAZ-CIP-AMP-SMX-TET(1)
CTX-CAZ-CIP-AMP-TET(1)
CTX-CAZ-CIP-NAL(1)
CTX-CIP-AMP-NAL-TET(1)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
Lithuania 81 CHL-CTX-CAZ-CIP-AMP-NAL-SMX(1) 26 32.1 14 17.3
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
CHL-CTX-CIP-AMP-SMX-TMP(1)
CTX-CAZ-CIP-AMP-COL-NAL-SMX-TET(1)
CTX-CAZ-CIP-AMP-NAL(6)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2)
CTX-CAZ-CIP-AMP-NAL-SMX-TMP(1)
CTX-CAZ-CIP-AMP-NAL-TET(1)
CTX-CAZ-CIP-AMP-SMX-TET(1)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX(1)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(5)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TMP(2)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2)
Netherlands 377 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1) 2 0.5
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TMP(1)
Poland 179 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1) 4 2.2 3 1.7
Resistant to
Resistant to both
MDR patterns of isolates resistant to both CIP both CIP and
CIP and CTX,
Country N and CTX CTX, applying
applying ECOFFs
(number of isolates) CBPs
N % Res N % Res
CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
CTX-CAZ-CIP-AMP-NAL-TET(2)
Portugal 201 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2) 10 5.0 3 1.5
CTX-CAZ-CIP-AMP-COL-NAL-SMX(1)
CTX-CAZ-CIP-AMP-NAL(1)
CTX-CAZ-CIP-AMP-NAL-SMX-TET(3)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
Slovakia 85 CHL-CTX-CAZ-CIP-AMP-NAL-SMX(1) 10 11.8 8 9.4
CTX-CAZ-CIP-AMP-NAL-SMX-TET(2)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CAZ-CIP-AMP-NAL-TET(2)
CTX-CIP-AMP-NAL-SMX-TMP(3)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
Slovenia 85 CTX-CAZ-CIP-AMP(1) 5 5.9
CTX-CAZ-CIP-AMP-NAL(1)
CTX-CAZ-CIP-AMP-NAL-SMX-TMP(1)
CTX-CAZ-CIP-AMP-TET(2)
Spain 170 CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1) 25 14.7 15 8.8
CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(1)
CTX-CAZ-CIP-AMP-NAL(5)
CTX-CAZ-CIP-AMP-NAL-SMX(1)
CTX-CAZ-CIP-AMP-NAL-SMX-TET(3)
CTX-CAZ-CIP-AMP-NAL-SMX-TET-TMP(2)
CTX-CAZ-CIP-AMP-NAL-SMX-TMP(3)
CTX-CAZ-CIP-AMP-NAL-TET(3)
CTX-CAZ-CIP-AMP-NAL-TET-TMP(1)
GEN-CHL-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX(1)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TET(1)
GEN-CTX-CAZ-CIP-AMP-NAL-SMX-TMP(1)
GEN-CTX-CAZ-CIP-AMP-NAL-TMP(1)
Total 3,311 194 5.9 87 2.6
(MSs 20)
N: number of isolates tested; CIP: ciprofloxacin; CTX: cefotaxime; ECOFFs: epidemiological cut-off values; % Res: percentage
of resistant isolates; CBPs: clinical breakpoints; CAZ: ceftazidime; NAL: nalidixic acid; AMP: ampicillin; TET: tetracycline; GEN:
gentamicin; CHL: chloramphenicol; COL: colistin; SMX: sulfamethoxazole; TMP: trimethoprim; MSs: Member States.: no
information available.
Compared with the proportion of resistant isolates at the EU level (computed as the fraction of the
total number of resistant isolates out of the total number of tested isolates in the group of reporting
MSs) typically presented in this EU Summary Report, the summary indicator better accounts for the
structure of the broiler populations within the EU i.e. the distribution of the broiler population per
reporting MS. More weight is given to the resistance observed in the broiler populations of important
size. Table 30 presents the resistance assessed by using totals and the summary indicator expressed
in percentages of resistant indicator E. coli isolates from broilers. Similar results are obtained,
although the summary indicator is generally slightly lower than the Total.
Table 30: Resistance in indicator E. coli from broilers assessed by the percentage of resistant
isolates (Total) and summary indicator (weighted mean of the proportions of resistant
isolates in the reporting MSs) in the EU, 27 MSs, 2014
Resistance levels among indicator Escherichia coli isolates from fattening turkeys
In 2014, resistance to ampicillin, sulfamethoxazole and tetracyclines in E. coli isolates from fattening
turkeys was generally very high among reporting MSs, ranging from 16.9% to 87.6%, whereas
resistance to chloramphenicol and trimethoprim was overall high at the reporting MSs level.
Conversely, resistance to azithromycin and gentamicin was low to moderate in most reporting
countries, with the notable exception of Italy and Romania, which reported high resistance. The
colistin resistance was generally recorded at low to very low levels. Resistance to ciprofloxacin and
nalidixic acid was high and very high among almost all reporting countries, ranging between 1.7% and
89.5%. The resistance to cefotaxime and ceftazidime was either not detected or reported at low levels
in all reporting countries.
Temporal trends in resistance among indicator Escherichia coli isolates from fattening turkeys
There were not enough data to present the trends in resistance to selected antimicrobials in indicator
E. coli from fattening turkeys from 2008 to 2014.
Spatial distribution of resistance among indicator Escherichia coli isolates from fattening turkeys
The spatial distribution of ciprofloxacin, nalidixic acid and cefotaxime resistance in indicator E. coli
from fattening turkeys is shown in Figure 74, Figure 75 and Figure 76, respectively. For nalidixic acid,
most countries reported moderate and high levels of resistance so the spatial pattern was less clear.
Figure 76 illustrates the variability in levels of cefotaxime resistance in E. coli across the EU and the
absence of a clear spatial distribution.
Table 31: Occurrence of resistance to selected antimicrobials in indicator Escherichia coli from fattening turkeys in reporting countries, in 2014
Country Ampicillin Azithromycin Cefotaxime Ceftazidime Chloramphenicol Ciprofloxacin Colistin(a)
N % Res N % Res N % Res N % Res N % Res N % Res N % Res
Austria 125 48.0 125 0.8 125 1.6 125 0.8 125 9.6 125 28.0 125 0
France 238 64.3 238 0.8 238 0.4 238 0.4 238 16.4 238 21.0 238 5.9
Germany 170 64.7 170 8.8 170 2.4 170 1.8 170 25.9 170 37.6 170 4.7
Hungary 170 61.2 170 1.8 170 1.8 170 1.8 170 18.8 170 62.9 170 0
Italy 170 78.8 170 3.5 170 1.2 170 1.2 170 26.5 170 60.0 170 22.9
Poland 170 75.9 170 1.2 170 2.4 170 1.8 170 22.9 170 70.0 170 2.9
Portugal 185 80.0 185 4.9 185 2.7 185 2.7 185 52.4 185 79.5 185 27.0
Romania 38 86.8 38 21.1 38 0 38 0 38 78.9 38 89.5 38 2.6
Spain 170 85.3 170 3.5 170 10.0 170 10.0 170 47.6 170 85.9 170 3.5
Sweden 59 25.4 59 0 59 1.7 59 1.7 59 3.4 59 3.4 59 0
United Kingdom 168 69.0 168 1.2 168 0 168 0 168 11.3 168 18.5 168 0
Total (MSs 11) 1,663 69.0 1,663 3.2 1,663 2.3 1,663 2.2 1,663 26.5 1,663 50.3 1,663 7.4
Figure 74: Spatial distribution of ciprofloxacin resistance among indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014
Figure 75: Spatial distribution of nalidixic acid resistance among indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014
Figure 76: Spatial distribution of cefotaxime resistance among indicator Escherichia coli from
fattening turkeys in reporting countries, in 2014
Multiple resistance among indicator Escherichia coli isolates from fattening turkeys
Eleven MSs reported isolate-based data from fattening turkeys. Around 14.0% of the isolates tested
were susceptible to the panel tested. In Sweden, 44.1% of the isolates were fully susceptible. Levels
of MDR (i.e. reduced susceptibility to three or more antimicrobial classes) ranged from moderate to
extremely high in reporting countries (Table COMESCHETURK). The frequency distributions
(Figure 77) showed that except Sweden all reporting countries detected MDR to as six antimicrobial
classes. Very few isolates (14 isolates out of 1,663 isolates tested) exhibited co-resistance to
cefotaxime and ciprofloxacin using either ECOFFs or CBPs as interpretive criteria (Table
COESCHETURK).
Sweden (N=59)
Austria (N=125) sus
Figure 77: Frequency distribution of Escherichia coli isolates completely susceptible and resistant to
one to 12 antimicrobials in fattening turkeys in MSs, 2014
Multi-/co-resistance patterns among indicator Escherichia coli isolates from fattening turkeys
Indicator E. coli isolates resistant to cefotaxime and ciprofloxacin using CBPs were observed in few
isolates from Germany, Italy, Poland and Spain, and ampicillin, sulfamethoxazole and tetracycline
resistance was often present in the isolates tested (Table 32 and Table MULTIESCHETURK). These
additional resistances (together with trimethoprim resistance in some cases) were noted in E. coli
isolates showing high-level ciprofloxacin resistance (Table CIPESCHETURK).
Resistance to colistin in E. coli from broilers and turkeys (see also main findings section)
Monitoring of colistin resistance has recently assumed greater importance with the discovery of
transferable resistance to colistin, conferred by the gene mcr-1 in China (Liu et al., 2015). The mcr-1
gene encodes a phosphoethanolamine transferase, which adds a phosphoethanolamine moiety to the
lipid A of the lipopolysaccharide component of the bacterial cell wall. Historically, resistance to colistin
was related to chromosomal alterations, which also affected lipid A and reduced the binding of colistin
to the cell wall, but these chromosomal alterations were not transferable. 2014 was the first year in
which the monitoring of colistin resistance in E. coli from animals was mandatory, and 0.9% and 7.4%
of the E. coli isolated from broilers and turkeys, respectively, were resistant to this antimicrobial.
Where colistin resistance is conferred by chromosomal alterations, then isolates with such alterations
either arise by mutation or through clonal expansion of resistant strains. In plasmid-mediated colistin
resistance, depending on the transmissibility and promiscuity of the plasmid and any other resistance
genes which are carried by the pasmid, then a different progression in the development of resistance
might be expected. In the case of promiscuous plasmids, this might involve rapid and extensive
dissemination to a wide range of E. coli strains.
As this report was being prepared, a number of countries worldwide reported the presence of mcr-1
in enterobacteriaceae recovered from humans, food or animals. Such reports demonstrated that mcr-1
was present in E. coli in food-producing animals (pigs and cattle) in Belgium in 2011-2012 (Malhotra-
Kumar et al., 2016) in France in veal calves in 2005 (Haenni et al., 2016) and in Germany in pigs in
2010 (Falgenhauer et al., 2016). Furthermore, the mcr-1 gene with or without the truncated mobile
genetic element ISApl1 in some cases occurred on a plasmid different from that reported in China,
which indicated that the mcr-1 gene has been transferred between different plasmids (Malhotra-
Kumar et al., 2016). These studies also showed that plasmids carrying mcr-1 had transferred between
different bacteria, because unrelated E. coli strains carried mcr-1 (Haenni et al., 2016). E. coli isolates
reported from pigs in Germany and veal calves in France also produced extended-spectrum beta-
lactamases (Falgenhauer et al., 2016; Haenni et al., 2016); although isolates from animals in Belgium
did not produce ESBLs, one which was sequenced showed multi-drug resistance (Malhotra-Kumar et
al., 2016). Although enterobacteriaceae from animals in Europe have not so far been reported which
carry mcr-1 and which are resistant to carbapenems, this has been reported in human clinical isolates
(Poirel et al., 2016).
3.3.3. Discussion
Studying the antimicrobial resistance of indicator commensal E. coli from animals and food provides
information on the reservoir of resistance genes occurring in those bacteria that could be transferred
to bacteria that are pathogenic for humans and/or animals. The occurrence of resistance to
antimicrobials in indicator E. coli is likely to depend on a number of factors including the selective
pressure exerted by use of antimicrobials in various food-producing animal populations; clonal spread
of resistant organisms; dissemination of particular genetic elements, such as resistance plasmids; and
the effects of co-selection in multiresistant organisms.
A total of 27 MSs and two non-MSs provided quantitative E. coli MIC data in 2014 for at least one of
the livestock species. Reported antimicrobial resistance data in E. coli isolates from food-producing
animals, derived mainly from active and representative monitoring programmes, were chiefly based
on randomised sampling performed at slaughterhouses. At the reporting MS group level, a high level
of microbiological resistance was observed to several antimicrobials among food-producing animals,
with some countries reporting a very or extremely high occurrence of such resistance. As resistance
levels tend to vary substantially between countries, the variation in resistance in broilers and fattening
turkeys observed between 2008 and 2014, at the overall MS group level, may partly result from
different MSs contributing to data as well as different production types of livestock being sampled.
Resistance levels were generally higher among E. coli isolates from broilers than isolates from
fattening turkeys. This was the fourth year that resistance data were reported separately for different
production types of Gallus gallus and it was the first year that mandatory AMR monitoring in indicator
E. coli broilers was in place.
Generally, similar microbiological resistance levels were identified for ampicillin, sulfamethoxazole and
tetracyclines, both in individual MSs and at the MS group level. These compounds are commonly used
therapeutically in animals and have been for many years; resistance to all three compounds often
features as a component of MDR patterns. At the MS group level, resistance to gentamicin was higher
in broilers (11.6%) than in fattening turkeys (10.0%). Gentamicin is an interesting antimicrobial
because there are differences in the degree of usage in different MSs of this and other antimicrobials
to which cross-resistance may occur (for example, apramycin).
Microbiological resistance to fluoroquinolones (ciprofloxacin) a class of antimicrobials critically
important in human medicine was found at higher levels in E. coli isolates from broilers than from
fattening turkeys. As resistance to fluoroquinolones commonly includes a mutational component, this
suggests either that E. coli isolates from broilers are exposed to greater selective pressure from the
overall use of fluoroquinolones or that the use of fluoroquinolones at a particular part of the
production pyramid (which selects for mutational resistance) causes resistance which is subsequently
disseminated to flocks lower in the pyramid by the spread and transfer of resistant bacterial clones.
Although the occurrence of high-level fluoroquinolone resistance is likely to be influenced by the
degree of fluoroquinolone usage, it is also likely to be influenced by the degree to which terminal
hygiene and disinfection procedures allow strains that have developed some resistance to persist and
colonise the subsequent group of animals. The occurrence of resistance to nalidixic acid was usually
similar to that for ciprofloxacin, suggesting that mutation was responsible for resistance. However, in
some MSs, the occurrence of resistance to ciprofloxacin was slightly higher than that obtained for
nalidixic acid, particularly in fattening turkeys. In these cases, mechanisms such as transferable
fluoroquinolone resistance conferred by qnr genes may have been responsible for resistance; as such,
plasmid-mediated mechanisms can result in this phenotypic pattern of resistance.
Microbiological resistance to third-generation cephalosporins (cefotaxime and ceftazidime) another
class categorised as critically important in human medicine was infrequently detected in 2014 in
E. coli from fattening turkeys where levels were < 2.3% in all reporting MSs. A number of reporting
MSs recorded high to moderate levels in E. coli from broilers, and resistance was typically higher in
isolates from broilers than in fattening turkeys. Monitoring using selective media for cefotaxime
resistance can detect cefotaxime-resistant E. coli present as a minor component of the total bacterial
flora in the test sample, which might only occasionally be detected by random sampling from non-
selective culture plates, and this will be performed from 2015, in accordance with Decision
2013/652/EU.
The levels of MDR21 in most reporting countries were relatively high in indicator E. coli isolates from
both broilers (8.195.3%) and fattening turkeys (10.289.5%), they were overall at very high levels
of resistance (54.3% in broilers and 58.9% in turkeys); as expected, the numbers of fully susceptible
isolates showed the inverse pattern. In general, the Nordic countries showed higher levels of full
susceptibility than other MSs; thus, in broilers, Denmark, Finland, Sweden and Norway were the only
reporting countries with > 70% full susceptibility, while, in fattening turkeys, Sweden and Austria
were the only reporting MSs with >30% full susceptibility. Considering clinical resistance, co-
resistance to cefotaxime and ciprofloxacin was detected at very low to high levels in broilers in 12 MSs
and at very low to low levels in four MSs in fattening turkeys in 2014. These E. coli isolates were
randomly chosen from non-selective culture plates and they may have limited direct relevance to
human medicine; however they provide an indication of the extent to which this combination of
resistance is occurring in the E. coli flora of animals in the different reporting countries.
This year, the MDR patterns shown by indicator E. coli from broilers and fattening turkeys from MSs
reporting isolate-based data have again been included in this report. Resistance to ampicillin,
ciprofloxacin, sulfamethoxazole, tetracyclines and trimethoprim was observed in 9.8% of all E. coli
isolates from broilers and was the predominant MDR pattern. Particular MDR patterns were
predominant in fattening turkeys, with one pattern occurring at a frequency of 15.9% amongst the
MDR patterns obtained. Two other MDR patterns each accounted more than 9.0% of the total MDR
isolates. The occurrence of these particular patterns might reflect spread of particular clones of
bacteria which exhibit that pattern of resistance or dissemination of plasmids carrying those
resistances and possibly being transmitted between different strains of E. coli. Strain typing of
selected E. coli isolates and detailed examination of E. coli plasmids would assist in differentiating
between clonal expansion of MDR E. coli strains and the spread of promiscuous MDR plasmids
between different E. coli strains by bacterial conjugation. The findings indicate some differences
between fattening turkeys and broilers in relation to the occurrence of multi-drug-resistant E. coli and
also reveal for broilers slight differences from the previous year, when no single MDR pattern was
predominant.
In broilers and also in fattening turkeys, ciprofloxacin resistance was particularly noted in MDR
patterns, and resistance to this compound can be mediated through chromosomal mutations or
through transferable mechanisms of resistance. Ciprofloxacin resistance was observed in 84.7% of
MDR E. coli isolates from broilers (2,386 out of 2,818), whereas ciprofloxacin resistance also occurred
frequently as a component of MDR in fattening turkeys and was present in 74.4% (728 out of 979) of
MDR E. coli isolates. Considering the resistance patterns occurring at a higher frequency in broilers,
and fattening turkeys, these did not generally include resistance to cefotaxime; however, cefotaxime
resistance did occur as a component of infrequent resistance patterns.
Tigecycline resistance was infrequently detected in E. coli isolates from broilers and turkeys. There are
technical issues in relation to testing tigecycline susceptibility and the isolates identified as showing
microbiological resistance will be subjected to further investigation at the EURL-AR. Marked
differences were evident between the results obtained for E. coli (where resistance was rare) and
Salmonella where resistance occurred more frequently and was associated with certain serovars, for
example, S. Infantis.
The most common pattern of multiple resistance in E. coli isolates from broilers that were co-resistant
to ciprofloxacin and cefotaxime was resistance to ciprofloxacin, nalidixic acid, cefotaxime, ceftazidime
and ampicillin. This occurred in 0.6% of the total number of E. coli isolates from broilers and was
detected in 11 MSs which reported co-resistant to ciprofloxacin and cefotaxime. A relatively simple
pattern of MDR was therefore shown by these isolates and it follows that only a limited number of
antimicrobials or antimicrobial classes is likely to be responsible for selection of isolates with this
resistance pattern; clonal spread of this MDR strain is a further possibility which could be investigated
through strain typing of these E. coli isolates. Co-resistance to ciprofloxacin and cefotaxime applying
microbiological breakpoints was less common in fattening turkeys (2.3% of all E. coli isolates) than in
broilers (5% of all E. coli).
21
Proportions of isolates showing reduced susceptibility to at least three antimicrobial classes according to epidemiological cut-
off values.
A variety of resistance patterns was observed in high-level ciprofloxacin-resistant E. coli isolates from
broilers and fattening turkeys, with each pattern occurring at a low frequency. This may suggest that,
in fattening turkeys and broilers, there is random mutation occurring in diverse strains of E. coli, which
are accumulating mutations and acquiring resistance. The possible occurrence of plasmid-mediated
quinolone resistance genes in those isolates, as suggested by the phenotypic patterns, calls for
confirmation.
Integrons can be associated with particular antimicrobial resistance genes and, in the Spanish study,22
both class 1 and class 2 integrons were detected in fattening turkeys and chickens. Class 1 integrons
classically carry the resistance gene sul1; additionally, both types of integrons in the Spanish study
often carried genes associated with streptomycin and trimethoprim resistance, whereas resistance
genes conferring chloramphenicol and gentamicin resistance were detected in the variable region of
class 1 integrons only. The widespread occurrence of integrons and their associated antimicrobial
resistance genes in E. coli from animals is likely to account for some of the resistance patterns (or
associations between resistances) which are evident in the MDR tables and probably explains why
sulfonamide, streptomycin and trimethoprim resistance are common components of MDR patterns.
The Spanish study also reported that the presence of integrons was associated with resistance to
amoxicillin (equivalent to ampicillin for resistance purposes) and tetracyclines. The common core
patterns of resistance to ampicillin, sulfamethoxazole, tetracyclines and trimethoprim (and
combinations thereof) frequently observed in the monitoring of E. coli isolates are probably therefore
related to the presence of integrons.
Full resistance to all of the antimicrobials in the test panel was not observed in any isolates from
broilers and fattening turkeys. Although no E. coli isolates from broilers or turkeys were resistant to
meropenem, further testing with the supplementary panel of cephalosporins and carbapenems
revealed that a number of isolates from broilers and a single isolate from turkeys were resistant to
ertapenem. The phenotypic resistance patterns were suggestive of permeability changes to the
bacterial cell wall (loss of porins) acting in association with AmpC or ESBL enzymes and are discussed
further in Chapter 3.6 on cephalosporin resistance.
22
High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain,
Vet Microbiol. 2004 Nov 30;104(1-2):1339.
A principal recommendation (EFSA, 2009a, 2009c and 2012b) is that monitoring of food-producing
animals, in particular intensively reared animals, is carried out periodically in conjunction with
systematic surveillance of MRSA in humans, so that trends in the diffusion and evolution of
zoonotically acquired MRSA in humans can be identified. Isolates representative of various animal and
food origins should be analysed for lineage determination, antimicrobial susceptibility and virulence-
associated traits. Monitoring of MRSA in animals and food is currently performed by MSs voluntarily. 23
23
The EFSAs assessment of the public health significance of MRSA in animals and food (EFSA, 2009c) and the Joint Scientific
Report of ECDC, EFSA and the European Medicines Agency (EMA) on MRSA in livestock, companion animals and food (EFSA,
2009a) provide more background information and recommendations on MRSA. These issues were reviewed in the recent
EFSA Scientific Report proposing technical specifications to improve the harmonisation of the monitoring and reporting of the
prevalence, genetic diversity and multiresistance profile of MRSA in food-producing animals and food thereof (EFSA, 2012b).
A number of different spa-types were reported (Table 34).The majority of isolates from pigs in
Switzerland were spa-type t034, with lower numbers of t011; both of these spa-types are associated
with MRSA CC398. The other spa-types detected in pigs in Switzerland were single isolates of t899,
which can be associated with ST9 or CC398 (Guardabassi et al., 2009), t2741, which can be
associated with CC11 or CC398 (EFSA, 2009b; Kck et al. 2013) and t208, which is associated with
ST49 in Switzerland (Overesch et al., 2011). Belgium provided spa-type data for MRSA isolates
recovered from Gallus gallus: t1985, which was detected in a single breeding flock of Gallus gallus in
Belgium, is associated with MRSA CC398, whereas t011, which is also associated with CC398, was
detected in laying hens.
24
The corresponding spa-type are presented in the footnote of.
Table 38: Occurrence of resistance (%) to selected antimicrobials in MRSA from food and animals,
2014
3.4.2. Discussion
Monitoring of MRSA in animals and food is currently voluntary and only a limited number of countries
reported MRSA data to EFSA in 2014. A number of MRSA strains have been detected in animals and
animal products, indicating that animals can acquire and disseminate MRSA strains other than those
which might strictly be regarded as LA-MRSA (Normanno et al., 2015; Battisti et al., 2010).
Although food is not currently considered to be a relevant source of MRSA infection or colonisation of
humans (EFSA, 2009c), the monitoring of MRSA in various food products performed in several MSs
consistently indicates that MRSA can be detected, quite frequently, in different types of food. Such
food included chicken, pork and meat from turkeys in 2014. It should be underlined that the
laboratory techniques used to detect MRSA employ selective bacterial culture and thus, very low levels
of contamination can be detected. LA-MRSA is considered a poor coloniser of humans and occurs
uncommonly in persons without direct or indirect contact with livestock or carcases derived thereof
(Graveland et al., 2010). Only low numbers of samples of some food were tested and prevalence
estimates are therefore likely to have wide confidence intervals, as a result of the small sample sizes.
Cross-contamination between carcases on slaughterhouse lines or during production processes may
result in a higher prevalence in meat produced from animals than in the animals themselves. It is also
noteworthy that prevalence measures may be obtained in relation to the contamination of individual
carcases, meat or other products, but for colonised animals, prevalence measures may be determined
at the flock or holding level, rather than by determining the status of individual animals.
Considering trends in the occurrence of MRSA in food, the monitoring of MRSA in meat products from
pigs in Spain showed an increase in prevalence of MRSA over the period 20122014, from 0% in 2012
to 8.5% in 2013 and 12.9% in 2014. In Germany, the prevalence of MRSA in fresh retail meat from
turkeys was assessed at similar levels of 37.7% and 42.5% in 2012 and 2014, respectively.
Switzerland reported spa-typing results for MRSA isolates from meat from broilers and most isolates
(19/22) belonged to spa-types associated with LA-MRSA CC398 (t011, t034, t571 and t899 25).
Although S. aureus belonging to spa-type t571 has been associated with severe disease in humans, a
particular clone of meticillin-susceptible S. aureus (MSSA) differing from that occurring in animals is
responsible (Cuny et al., 2013). The spa-type t571 isolates reported by Switzerland are meticillin-
resistant and are therefore likely to be related to LA-MRSA, rather than the human MSSA t571 clone.
Three isolates from broiler meat at retail were spa-type t032, which is a spa-type associated with the
HA-MRSA, EMRSA-15, belonging to CC22. Spa-type t032 is therefore usually associated with a
healthcare-associated strain of MRSA, not commonly reported from food-producing animals.
Contamination of meat with HA-MRSA from persons in contact with the meat at some point is a
possible explanation for its occurrence.
In food-producing animals in 2014, most of the MRSA spa-types detected were associated with LA-
MRSA CC398. Switzerland detected single isolates of spa-types t899 and t2741, which can also be
associated with CC398, but which may also associated with either ST9 or CC11, respectively. Although
the likelihood is that these isolates were also associated with CC398, the findings illustrate the
limitations of spa-typing as a single method of definitively assigning all of the animal isolates which
were recovered by reporting countries to particular MRSA lineages. Spa-type t208, which is associated
with ST49 in Switzerland, has been considered to have emerged in the Swiss fattening pig population
by acquisition of the SCCmec element by MSSA belonging to ST49 (Overesch et al., 2011). Switzerland
has performed annual surveillance for MRSA in pigs since 2009 (Table 37: ). MRSA ST49 has persisted
in pigs over this monitoring period and, although it was initially reported from seven different farms, it
has not subsequently increased in prevalence, whereas it is noteworthy that those spa-types
associated with CC398 have shown a steady increase in prevalence. Data relating to colonisation by
MRSA CC398 in humans in European countries show a similar trend in some countries, for example,
an increase in MRSA CC398 cases as a proportion of all MRSA cases detected in nasopharyngeal
swabbing of patients at 39 hospitals from 14% in 2008 to 29% in 2012 was noted in north-western
Germany (Kck et al., 2013). In the Netherlands, 15% of human carriers of MRSA CC398 do not
report direct contact with pigs or veal calves; indirect transmission from animals or direct transmission
from colonised humans are possible sources (Lekkerkerk et al., 2015). Although LA-MRSA CC398 is
considered a poor coloniser of human (Graveland et al., 2010), it can cause serious, fatal infections in
humans, especially in patients who are prone to acquire staphylococcal infections (Berning et al.
2015). Berning et al. reported case details of two fatal infections, both of which occurred in persons
with direct links to pig farms or pig farming.
Considering the three broad epidemiological classes of MRSA (LA-MRSA, HA-MRSA and CA-MRSA),
spa-typing data confirms that spa-types associated with CC398 were most frequent and therefore,
livestock-associated MRSA remained the type of MRSA most frequently detected in food-producing
animals in 2014. Spa-types associated with healthcare-associated MRSA were much less frequent and
those associated with CA-MRSA were not reported. Where spa-typing data are not available, the
susceptibility of isolates may give some indication of the type of MRSA likely to have been detected,
because livestock-associated MRSA belonging to CC398 are usually resistant to tetracycline (Cromb
et al., 2013), although this is of course not a definitive characteristic because tetracycline resistance
also occurs in other strains of MRSA. Susceptibility data for MRSA isolates were provided by Belgium
and Switzerland who did not detect resistance to either vancomycin or linezolid, important
antimicrobials for treatment of human patients. The high proportion of MRSA isolates from pigs
showing resistance to tiamulin and trimethoprim presumably reflects the relatively common usage of
these compounds in pig medicine in many European countries.
Norway tested a large number of pig herds (N=986) in 2014, as part of a surveillance and eradication
programme for LA-MRSA (outlined at http://www.vetinst.no/eng/Surveillance-programmes/Swine-
MRSA). National eradication programmes for LA-MRSA have not been attempted in other European
countries. Norway has consistently demonstrated a very low/zero prevalence of MRSA-positive pig
25
Spa-type t899 can be associated with either MRSA ST9 or CC398.
herds in surveillance performed since 2008 and this situation is likely to be favourable to achieving the
goal of eradicating and then maintaining freedom from LA-MRSA. The eradication programme involves
slaughter and depopulation of affected herds, followed by thorough cleaning and disinfection and then
re-stocking with pigs free from LA-MRSA.
S. aureus isolates belonging to CC398 can be divided into human and animal lineages based on
characteristics including susceptibility to meticillin and tetracyclines (animal lineages are resistant;
human lineages are susceptible) and possession of the SA3 prophage, scn and chp virulence genes,
features which have been associated with the meticillin-susceptible lineages of CC398 affecting
humans (Smith and Wardyn, 2015, Chroboczek et al. 2013). The results reported here relate to MRSA
isolates from animals and food and considering the rapid developments which have occurred in recent
years relating to the occurrence of MRSA in animals and the emergence of LA-MRSA, it seems likely
that further evolution will occur. Spa-typing provides a convenient method for preliminary
characterisation of isolates described in this report, but may not always contain sufficient information
to fully interpret the significance of isolates.
Rationale for the choice of certain substances included in the supplementary panel
Cefotaxime and ceftazidime have been included in the supplementary panel because, although
most ESBL confer resistance to both compounds, some ESBL primarily confer resistance to one or
the other compound.
Confirmatory synergy testing has been also foreseen so that a presumptive ESBL phenotype may
be identified.
Cefoxitin has been also included so that a presumptive AmpC phenotype may be identified.
Meropenem, imipenem and ertapenem have been included so that putative carbapenemase
producers may be identified.
Temocillin (6--methoxy-ticarcillin) efficacy is unaffected by most ESBL and AmpC enzymes and
this substance may be particularly useful in human medicine to treat urinary tract infections caused
by ESBL-producing Gram-negative organisms (Livermore and Tulkens, 2009). Susceptibility to
temocillin enables further phenotypic characterisation of carbapenemases.
From the results of such further testing, it has thus been possible to infer the presumptive class of
beta-lactamase enzyme which was responsible for conferring the phenotypic profile of resistance to
third-generation cephalosporins or meropenem detected, providing additional epidemiological
information. This monitoring primarily addressed in this chapter was performed in accordance with the
legislation and did not utilise selective primary isolation media containing cephalosporins so the results
generally relate to organisms selected at random from primary culture media.
In 2014, the specific monitoring of ESBL-/AmpC-/Carbapenemases-producing E. coli (by using
selective media containing cephalosporins) was also performed on a voluntary basis by a limited
number of reporting countries. The corresponding results have also been briefly presented below, and
the results of the routine and specific monitoring were put in perspective, if possible. Italy also
reported results of a specific monitoring of carbapenemase-producing microorganisms (by using
selective media containing carbapenems), performed voluntarily.
Resistance levels to carbapenems in Salmonella isolated from meat from broilers and turkeys
None of the Salmonella isolates from meat from broilers or turkeys were microbiologically resistant to
meropenem, ertapenem or imipenem.
Resistance levels to carbapenems in Salmonella from flocks of broilers, laying hens and turkeys
None of the Salmonella isolates from broiler, laying hen and turkey flocks which were subjected to
supplementary testing were microbiologically resistant to ertapenem, imipenem or meropenem.
Resistance levels to cefotaxime and ceftazidime in Salmonella from laying hen flocks
The levels of resistance in laying hen flocks were generally lower than those reported in broiler flocks.
In Salmonella spp. from laying hens, only three MSs (France, Poland and Romania) detected
resistance to third-generation cephalosporins out of the 15 reporting MSs, respectively.
Considering isolates from laying hens resistance to cefotaxime and ceftazidime in S. Enteritidis was
detected by Poland (Table ENTERLAYD). S. Typhimurium isolates from laying hens
(Table TYPHILAYD) were tested by 17 MSs; none of the reporting countries detected resistance to
cefotaxime or to ceftazidime in S. Typhimurium.
Resistance levels to cefotaxime and ceftazidime in Salmonella from fattening turkey flocks
There were no Salmonella isolates from turkey flocks which were resistant to cefotaxime or
ceftazidime in the nine reporting MSs in 2014 (Table SALMFATTURKD) and therefore, no
supplementary beta-lactam susceptibility testing was performed on isolates.
Table 39: Occurrence of resistance to beta-lactam compounds in Salmonella spp. isolates from
broilers, laying hens and meat from broilers collected within the routine monitoring and
subjected to supplementary testing (panel 2) in 2014
Table 40: Presumptive ESBL and AmpC phenotypes identified in Salmonella spp. isolates from broilers, laying hens and meat from broilers collected within
the routine monitoring and subjected to supplementary testing (panel 2) in 2014(a)
Resistance to cefotaxime, ceftazidime and carbapenem compounds, and presumptive ESBL and AmpC
phenotypes identified in E. coli isolates from fattening turkeys
Data on resistance in indicator E. coli isolates from fattening turkeys were reported by 11 reporting
MSs. The levels of resistance recorded for third generation cephalosporins were generally low;
Romania and the United Kingdom did not detect any resistance. Overall, resistance levels in reporting
countries were lower in fattening turkeys than in those from broilers, at 2.3% for cefotaxime and
2.2% for ceftazidime (Table ESCHETURK and Table 43).
A single ertapenem-resistant indicator E. coli isolate was reported by France and this isolate exhibited
a presumptive AmpC phenotype (Table 44). Loss of porins in conjunction with AmpC enzyme
production is therefore considered to account for resistance to ertapenem in the absence of resistance
to the other carbapenems tested.
Indicator E. coli isolates with a presumptive ESBL phenotype were detected in fattening turkeys in six
MSs and three non-MSs. Significant numbers of isolates showed synergy with cefotaxime only. The
proportion of all E. coli isolates from broilers with a presumptive ESBL phenotype was low or very low
in most countries, except in Spain where 10% of the E. coli sampled exhibited a presumptive ESBL
phenotype. Three MSs reported E. coli isolates with a presumptive AmpC phenotype in fattening
turkeys, although those isolates accounted for less than 2% of indicator E. coli investigated in each
MS. No presumptive ESBL and AmpC phenotype was detected in fattening turkeys (Table 44).
Table 41: Occurrence of resistance to beta-lactam and carbapenem compounds in indicator E. coli isolates from broiler flocks collected within the routine
monitoring and subjected to supplementary testing (panel 2) in 2014
Country Total number Number subjected to supplementary testing and number resistant
of Cefotaxime Ceftazidime Cefoxitin Cefepime Ertapenem Temocillin
E. coli tested N n Res N n Res N n Res N n Res N n Res N n Res
Austria 176 2 2 2 2 2 0 2 2 2 0 2 0
Belgium 158 13 13 13 12 13 5 13 11 13 0 13 0
Croatia 170 1 1 1 1 1 0 1 1 1 0 1 0
Cyprus 87 35 28 35 26 35 15 35 25 35 0 35 0
Czech Republic 196 2 2 2 2 2 0 2 2 2 0 2 2
Estonia 71 3 3 3 1 3 2 3 1 3 0 3 0
France 226 9 9 9 9 9 0 9 9 9 0 9 0
Germany 227 5 3 5 3 5 1 5 3 5 0 5 0
Greece 172 5 5 5 5 5 2 5 5 5 0 5 0
Hungary 170 5 5 5 5 5 3 5 4 5 0 5 0
Ireland 167 7 7 7 6 7 2 7 7 7 0 7 0
Italy 170 11 11 11 9 11 3 11 11 11 0 11 0
Latvia 147 48 45 48 43 48 15 48 40 48 1 48 0
Lithuania 85 32 27 32 31 32 20 32 24 32 3 32 0
Netherlands 377 10 10 10 10 10 0 10 10 10 0 10 0
Poland 179 4 4 4 4 4 3 4 4 4 1 4 0
Portugal 201 11 11 11 11 11 1 11 11 11 0 11 0
Romania 859 15 15 15 15 15 8 15 10 15 0 15 0
Slovakia 86 16 11 16 6 16 4 16 11 16 1 16 0
Slovenia 85 8 8 8 8 8 7 8 6 8 1 8 0
Spain 170 25 25 25 25 25 7 25 25 25 2 25 0
Total (21 MSs) 4,179 267 245 267 234 267 98 267 222 267 9 267 2
Norway 205 3 3 3 3 3 3 3 0 3 0 3 0
No E. coli isolates from broilers were resistant to meropenem.
Interpretive cut-off applied for temocillin: > 32 mg/L.
ECOFFs: epidemiological cut-off values; N: number of the isolates tested; n Res: number of the isolates resistant; MSs: Member States
Table 42: Presumptive ESBL and AmpC phenotypes identified in indicator E. coli isolates from broiler flocks collected within the routine monitoring and
subjected to supplementary testing (panel 2) in 2014(a)
Country Total number Number of Presumptive Resistance Phenotype
of E. coli E. coli with (b) ESBL with clavulanic-SYN ESBL with clavulanic-SYN
ESBL AmpC(e) AmpC + ESBL(f)
tested supplementary only for CTX(c) only for CAZ(d)
testing n %(g) n % (g)
n %(g) n %(g) n %(g)
Austria 176 2 2 1.1 2 1.1
Belgium 158 13(h) 7 4.4 2 1.3 1 0.6 5 3.2
Croatia 170 1 1 0.6 1 0.6
Cyprus 87 35 13 14.9 8 9.2 8 9.2 7 8.0
Czech Republic 196 2(i) 2 1.0
Estonia 71 3(h) 1 1.4 1 1.4
France 226 9 9 4.0 3 1.3 1 0.4
Germany 227 5 3 1.3 2 0.9
Greece 172 5 3 1.7 2 1.2 2 1.2
Hungary 170 5 2 1.2 1 0.6 1 0.6 3 1.8
Ireland 167 7(h) 4 2.4 3 1.8 2 1.2
Italy 170 11(i) 8 4.7 2 1.2 1 0.6 3 1.8
Latvia 147 48 30 20.4 8(j) 5.4 8 5.4 7 4.8 8 5.4
Lithuania 85 32(j) 12 14.1 5 5.9 3 3.5 19(j) 22.4 1 1.2
Netherlands 377 10 10 2.7 4 1.1
Poland 179 4 1 0.6 3(j) 1.7
Portugal 201 11 10 5.0 1 0.5 1 0.5
Romania 859 15(h) 6 0.7 8 0.9
Slovakia 86 16 9 10.5 6 7.0 2(j) 2.3
Slovenia 85 8 1 1.2 7(j) 8.2
Spain 170 25(i,j) 18 10.6 2 1.2 3 1.8 4 2.4
Total (21 MSs) 4,179 267 152 3.6 51 1.2 17 0.4 73 1.7 20 0.5
ESBL: extended spectrum beta-lactamase; n= isolates with this phenotype; %: percentage of isolates from the total tested; SYN: synergy; CTX: cefotaxime; CAZ: ceftazidime; MSs: Member States.
(a): According to EUCAST Guidelines (EUCAST, 2013), only isolates showing an MIC > 1 mg/ml for cefotaxime and/or ceftazidime (screening breakpoint) were considered (see Chapter 1.2.5).
(b): All isolates with an ESBL phenotype, i.e. showing clavulanate synergy with cefotaxime or ceftazidime or synergy with both compounds.
(c): Isolates showing synergy with cefotaxime only, suggesting the presence of an ESBL with cefotaximase activity.
(d): Isolates showing synergy with ceftazidime only, suggesting the presence of an ESBL with ceftazidimase activity.
(e): Isolates with microbiological resistance to cefoxitin.
(f): Isolates showing synergy with cefotaxime or ceftazidime and with microbiological resistance to cefoxitin. nel 1).
(g): Percentage of the total number of E. coli isolates tested (with panel 1).
(h): Isolates microbiologically resistant to cefotaxime and/or ceftazidime but with MIC =< 1 mg/L for both antimicrobials (suggesting the presence of other mechanisms, but not further classified)
were reported by Belgium (1 isolate), Romania (1), Estonia (2) and Ireland (1).
(i): Molecular data were reported by the Czech Republic, Italy, and Spain. Almost all isolates were reported as positive the ESBL CTX-M, SHV, TEM- or AmpC CMY-2 encoding genes tested,
according to their phenotypes. For Italy, one isolate reported positive for SHV showed an MIC = 16 mg/L (suggesting the presence of a chromosomal AmpC) but no synergy, thus was classified
in the AmpC-phenotype group and not in the putative ESBL- nor ESBL+AmpC-phenotypes ones. For Spain, the isolates classified in the ESBL+AmpC phenotype groups, showed a cefoxitin
MIC = 16 mg/L, suggesting the presence of cAMPc together with the CTX-M reported. Two of the three Spanish isolates exhibiting AmpC phenotype were reported as CMY-2 positive, but, for
the third isolate placed in this group because of exhibiting an MIC = 64 mg/L for cefoxitin and no synergy, no CMY-2 encoding gene was reported.
(j): Included isolates with ertapenem resistance (MIC = 0.12-0.25 mg/L).
Table 43: Occurrence of resistance to beta-lactam and carbapenem compounds in indicator E. coli isolates from fattening turkeys collected within the
routine monitoring and subjected to supplementary testing (panel 2) in 2014
Country Total number Number subjected to supplementary testing and number resistant
of E. coli tested Cefotaxime Ceftazidime Cefoxitin Cefepime Ertapenem Temocillin
N n Res N n Res N n Res N n Res N n Res N n Res
Austria 125 2 2 2 1 2 0 2 2 2 0 2 0
France 238 1 1 1 1 1 1 1 1 1 1 1 0
Germany 170 6 4 6 3 6 0 6 4 6 0 6 0
Hungary 170 4 3 4 3 4 2 4 2 4 0 4 0
Italy 170 2 2 2 2 2 0 2 2 2 0 2 0
Poland 170 3 2 3 2 3 3 3 3 3 0 3 0
Portugal 185 5 5 5 5 5 0 5 5 5 0 5 0
Spain 170 17 17 17 17 17 0 17 17 17 0 17 0
Sweden 59 1 1 1 1 1 0 1 0 1 0 1 0
Total MSs (9) 1,457 41 37 41 35 41 6 41 36 41 0 41 0
No E. coli isolates from fattening turkeys were resistant to imipenem or meropenem.
Interpretive cut-off applied for temocillin: > 32 mg/L.
ECOFFs: epidemiological cut-off value; MSs: Member States.
Table 44: Presumptive ESBL and AmpC phenotypes identified in indicator E. coli isolates from fattening turkeys collected within the routine monitoring and
subjected to supplementary testing (panel 2) in 2014(a)
Table 45: Prevalence of carbapenemase-producing E. coli from broilers and fattening turkeys
collected within the specific carbapenemase-producing microorganisms monitoring in
Italy in 2014
This study provides baseline information of utmost interest, as in Italy, CPE-R Enterobacteriaceae in
humans are widespread and are currently considered a major burden among healthcare-associated
infectious diseases.
Table 46: Prevalence of ESBL-/AmpC-producing E. coli from broilers and fattening turkeys within
the specific ESBL-/AmpC-producing E. coli monitoring in Italy in 2014
It should be noted that, when using selective culture methods, the occurrence of ESBL/AmpC-
producing E. coli in broilers and fattening turkeys is assessed with much greater sensitivity than when
using non-selective culture methods. Considering randomly selected isolates of indicator commensal
E. coli (n=170) from the same caecal samples, cultured on non-selective media, the occurrence of
ESBL/AmpC-producing E. coli was 6.47% (11/170) in broilers and 1.18% (2/170) in turkeys,
respectively.
The difference is most likely explained by the fact that the ESC-R population may be still sub-
dominant among the E. coli populations in the gut flora of these food-producing animals, so that the
probability of randomly picking an ESC-R E. coli from non-selective agar plates is not high for the
majority of samples tested.
Third- and fourth-generation cephalosporins have never been licensed for use in poultry in Italy, and
off-label use is currently prohibited, according to the EU legislation. Selection pressure exerted by the
use of high amounts of other antimicrobial classes ( e.g. tetracyclines, sulfonamides, aminopenicillins,
(fluoro)quinolones), may also contribute to co-selection of ESC-R, since ESC-R isolates can show
multiple drug resistance.
Monitoring of ESBL-/AmpC-/carbapenemase-producing Salmonella at slaughter
Cultures for Salmonella spp. according to the ISO standards were also performed on the samples
collected according to Commission implementing Decision 2013/652/EU. All isolates were serotyped
and susceptibility tested, with molecular confirmation of phenotype by PCR.
Table 47: Prevalence of ESBL-/AmpC-producing Salmonella from broilers and fattening turkeys
within national specific ESBL-/AmpC-producing Salmonella monitoring in Italy in 2014
A total 89 isolates from broilers were available for AST testing. No CPE-R Salmonella was detected
(prevalence: 0.0%, 95% CI: 0.0, 0.52%). ESC-R isolates comprised 3.37% of the total (3/89), and
were multiresistant serovar Infantis isolates. This serovar represented 75% of all isolates detected in
the survey. S. Infantis is also the most frequent serovar reported as ESC-R among isolates tested in
the national control programme (NCP) in broiler chicken (27.27% ESC-R in 2014, the vast majority of
which are due to an emerging ESBL, CTX-M-1-producing S. Infantis clone).
A total 145 isolates from turkeys were available for AST testing. ESC-R isolates were 0.69% (1/145), a
low figure which is in agreement with susceptibility data from the NCP in turkeys.
Although the data sets from the two different types of study (survey at slaughter vs. NCP) are not
directly comparable, monitoring trends in AMR in Salmonella spp. (including MDR and resistance to
Critically Important Antimicrobials), using both approaches (Census and Objective sampling strategies)
may contribute to provide a more accurate picture of the epidemiology of AMR in Salmonella spp. in
Italy.
Table 48: Occurrence of resistance to selected antimicrobials in Escherichia coli from broilers and fattening turkeys in reporting countries collected within
thespecific ESBL-/Ampc-/carbapenemase-producing monitoring (Panel 1), in 2014
Table 49: Occurrence of resistance to selected antimicrobials in Escherichia coli from broilers and fattening turkeys in reporting countries collected within
the specific ESBL-/Ampc-/carbapenemase-producing monitoring (Panel 1), in 2014
Table 50: Presumptive ESBL and AmpC phenotypes identified in E. coli isolates from meat from broilers, broilers and fattening turkeys collected within the
specific ESBL-/Ampc-/carbapenemase-producing monitoring and subjected to supplementary testing or molecular typing confirmation in 2014 (a)
Table 51: Resistance (%) to cefotaxime and ceftazidime in Salmonella spp. and indicator E. coli isolates in MSs in 2014 testing both bacterial species in
broilers or fattening turkeys
3.5.5. Discussion
Third-generation cephalosporins are antimicrobials of particular importance because they are
frequently used as the first-line treatment in invasive Gram-negative infections, for example infections
caused by E. coli or Salmonella. In 2014, as in the previous years, resistance to third-generation
cephalosporins was generally detected at low levels in Salmonella and indicator E. coli isolates
recovered from broilers, laying hens and fattening turkeys and meat thereof.
In most MSs, the prevalence of resistance to cefotaxime in both Salmonella spp. and E. coli was equal
to that observed for ceftazidime. Although resistance assessed using ECOFFs tends to usually detect
resistance to both compounds, this is not always the case and differences in resistance to each
compound may be observed, reflecting whether the ESBL enzyme conferring resistance is primarily a
cefotaximase or a ceftazidimase. ESBLs belonging to the CTX-M family (primarily, although not
entirely, cefotaximases) are currently the most important types of ESBL in both animals and humans
in the majority of MSs. EFSA recommended that both cefotaxime and ceftazidime should be included
in the harmonised mandatory monitoring to ensure optimal detection of all ESBLs (including also
SHV-, TEM- and OXA-variants) (EFSA, 2012a), and this was implemented in 2014, as surveillance
procedures should anticipate possible changes in the status of different ESBL enzymes. The value of
this approach is evident in the cephalosporin resistance figures presented for broilers, where some
isolates were detected which showed synergy with either cefotaxime or ceftazidime alone.
The results have been presented by animal production type. Differences in the occurrence of
resistance may be related to husbandry methods, age or stage of production, the degree of
antimicrobial usage or the influence the structure of the particular livestock industry may have on
clonal spread of resistant organisms. Occurrence of resistance to cefotaxime or/and ceftazidime in
Salmonella spp. was higher in broilers than in laying hens (whenever resistance was detected) for all
MSs (9/22 vs. 3/15 reporting MSs). Laying hens tend to be infrequently treated with antimicrobials,
especially once in lay. The three MSs reporting cefotaxime or ceftazidime resistance in Salmonella spp.
from laying hens, each reported only single isolates of serovars Enteritidis, Paratyphi and Cerro. The
situation differed in relation to Salmonella spp. resistant to third-generation cephalosporins in broilers,
where, of the nine MSs reporting resistant isolates, only two reported single isolates the remainder
detected more than one isolate and Italy ( S. Infantis) and the Netherlands (S. Heidelberg) in
particular reported multiple isolates of the same serovar, indicating likely clonal dissemination of these
serovars in broilers in those MSs. S. Enteritidis from broilers and layers were mostly susceptible to
cefotaxime and ceftazidime from most MSs, with the exception of single S. Enteritidis isolates from
broilers from Portugal and from layers from Poland. Malta reported isolates resistant to ceftazidime,
but susceptible to cefotaxime, in broilers, suggesting that a ceftazidimase enzyme may have been
present. Salmonella spp. resistant to cefotaxime was most frequently observed in broilers and the
proportion of MSs observing any degree of resistance was higher than that for fattening turkeys
where no resistance to third-generation cephalosporins was detected. Although resistance to third-
generation cephalsporins was not detected in Salmonella spp. from fattening turkeys, only nine MSs
reported results for turkeys, whereas 22 MSs reported results for Salmonella spp. from broilers. Some
Salmonella serovars have particular public health significance because they either are common causes
of human salmonellosis or have acquired resistance to a large number of different antimicrobial
compounds (or even exhibit both of these traits). Resistance to third-generation cephalosporins was
detected in a number of serovars of particular public health importance, including S. Typhimurium,
S. Enteritidis and S. Infantis.
Although thorough cooking and appropriate food hygiene procedures kill any bacteria present on food
and prevents cross-contamination of foods with resistant or susceptible bacteria, it is highly desirable
that the level of resistance in zoonotic organisms is very low or zero, especially in relation to important
antimicrobials for human treatment. Among the strains of E. coli occurring in animals, some may be
able to cause infections in humans (many will be largely harmless animal commensals) and some,
although they are primarily commensals of animals, may be able to transiently or permanently
colonise the human intestine. During transient colonisation or passage through the human intestine,
E. coli may be able to exchange their resistance plasmids with the commensal E. coli flora of humans.
Therefore, it is also desirable that resistance to important antimicrobials for human treatment is also
very low or zero in animal strains of E. coli, which might otherwise form a reservoir of resistance
genes.
Considering the 4,179 E. coli isolates reported from broilers, 5% showed co-resistance to cefotaxime
and ciprofloxacin using ECOFFs and 2.3% using clinical breakpoints. Figures for the 2,293 Salmonella
spp. isolates from broiler flocks were rather similar, with 2.3% co-resistance to cefotaxime and
ciprofloxacin detected using ECOFFs and 2.0% co-resistance detected using clinical breakpoints. In
laying hen flocks, where E. coli data were not available, co-resistance in Salmonella occurred at the
much lower level of 0.3%. Differences in the pattern of usage of antimicrobials in broiler and laying
hen flocks may account for the lower level of co-resistance observed in Salmonella isolates from laying
hens. Similarly, of 1,398 E. coli isolates from fattening turkeys, the figures were 2.3% and 1% for co-
resistance to cefotaxime and ciprofloxacin using ECOFFs and clinical breakpoints, respectively,
whereas co-resistance was not detected in Salmonella spp. from turkeys. These differences between
E. coli and Salmonella spp. in relation to the observed levels of resistance to cephalosporins and of co-
resistance to cefotaxime and ciprofloxacin may relate to a number of factors. Clonal expansion of
Salmonella spp. is suspected in isolates from broilers from Italy and the Netherlands, where one
Salmonella serovar is dominant among those showing resistance. Clonal expansion will be more
readily detected in Salmonella than in E. coli because of the primary culture methods which are used,
in which E. coli are selected at random from the total E. coli population which is present.
The emerging serovar S. Kentucky was the only serovar to show high-level resistance to ciprofloxacin,
and resistance to cefotaxime and ceftazidime, with a single isolate from broilers in Spain detected with
such resistance. Resistance to both first-line compounds used for treatment of invasive salmonellosis
is undesirable because both first-line treatments are likely to be ineffective.
Third-generation cephalosporin resistance in Salmonella was very low or absent for most of the MSs,
but when present, there were some differences on the resistance mechanisms found depending on
the animal species. In Salmonella from laying hen flocks, AmpC enzyme producers were detected at a
very low level, whereas in Salmonella from broiler flocks, ESBL enzyme producers predominate in
most MSs, although AmpC enzyme producers were majority in the Netherlands, but also occurred in
some other MSs. The occurrence of only a few serovars having acquired these types of resistance
(S. Infantis, S. Heidelberg and S. Java) may be related to the prevalence of these serovars in those
MSs, where resistance was detected or may be related to particular features which have allowed them
to develop resistance or enabled them to spread. In E. coli from both broilers and fattening turkeys,
isolates with a presumptive ESBL phenotype were more common than isolates with a presumptive
AmpC phenotype. Ertapenem resistance was observed in some isolates with an ESBL or AmpC
phenotype and this is presumed to be related to ESBL or AmpC enzyme production in conjunction with
loss of porins.
Temocillin (6--methoxy-ticarcillin) was included in the supplementary panel of antimicrobials for any
isolates showing resistance to cefotaxime, ceftazidime or meropenem in 2014. Temocillin can allow
further phenotypic characterisation of carbapenemase-producing isolates26. Temocillin is unaffected by
most ESBL and AmpC enzymes and may be particularly useful in human medicine to treat urinary tract
infections caused by ESBL-producing Gram-negative organisms (Livermore and Tulkens, 2009).
Resistance to temocillin in ESBL- and AmpC-producing E. coli detected in poultry was rare and was not
observed in E. coli from fattening turkeys in any MS. In E. coli from broilers, it was only detected in
one MS in two isolates, which were both phenotypically ESBL-producers. The significance of E. coli in
poultry and other food-producing animals as a direct cause of extra-intestinal pathogenic E. coli
infections in humansis the subject of debate (Blanger et al., 2011). Irrespective of any possible direct
significance of these organisms for humans, resistance in commensal E. coli in animals constitutes a
reservoir of resistance genes and a low prevalence of cephalosporin resistance is therefore desirable.
For the routine AMR monitoring in commensal indicator E. coli, the examination of a single randomly-
selected E. coli isolate from non-selective culture plates was performed. This approach enables the
assessment of the proportion of randomly selected E. coli that is resistant to cephalosporins, as
categorized as presumptive ESBL/ampC/carbapenemase producers. It provides a lower degree of
sensitivity, particularly where ESBL-producing E. coli constitutes a small proportion of the total E. coli
flora, than that obtained using specific monitoring based on selective media. The approach is useful
for consumers risk assessment, as it is consider that E. coli will be transferred along the food chain in
a random fashion (EFSA, 2012a).
26
For example, those isolates producing the enzyme OXA-48 in which high-level resistance to temocillin can be observed
(Woodford et al., 2013).
Conversely, for the specific ESBL/AmpC/carbapenemase monitoring, culture methods using a non-
selective enrichment and a selective medium for the detection of producer E. coli (protocol
recommended by the EURL-AR) shall be used. The method would allow the detection of ESBL/AmpC
within samples (determination of the proportion of samples contaminated with ESBL-/AmpC-
/carbapenemases-producing E. coli). The sensitivity to detect the producer E. coli by this approach is
higher than that obtained when performing the (random) routine monitoring, especially when
investigating populations with a low prevalence of ESBL-producing E. coli. If large numbers of AmpC-
producing E. coli are present in samples, they may obscure the concomitant presence of ESBL-
producing E. coli in the same samples. It should be taken into account that for MDR data analyses,
only a subpopulation of E. coli would be represented (EFSA, 2012a).
Because this report covers only phenotypic monitoring, it is not possible to determine the class or
exact type of beta-lactamase enzyme which is responsible for conferring the resistance detected to
third-generation cephalosporins. Categorising isolates which are resistant to third-generation
cephalosporins and/or carbapenems according to their presumptive ESBL, AmpC and or
carbapenemase phenotype provides useful epidemiological information on the reservoirs of the
different types of resistance present in E. coli in different food-producing animal populations and
categories of foodstuffs. For those countries providing molecular data on the occurrence of selected
acquired genes (i.e. blaCTX-M, blaSHV ESBLs, blaCMY-2), the classification of the isolates according to their
presumptive phenotypes based on the EUCAST criteria (EUCAST, 2013) was supported in most of the
cases (6/151 isolates) by the genotypic findings reported by these MS, underlining the
appropriateness of the criteria applied. The main differences were found for the isolates classified as
presumptive ESBL + AmpC-producers for which the reported MIC values for cefoxitin (low resistance,
values close to the ECOFF) could be related, at least in E. coli, with the putative expression of intrinsic
AmpC genes (Table 40, Table 42, Table 44 and Table 49).
Regarding carbapenem non-susceptibility and detection of putative carbapenemase-producers within
indicator E. coli and/or Salmonella, after validation of data (retesting of antimicrobial susceptibility and
species identification by several MSs), none of the data reported for the isolates collected within the
routine monitoring suggested the presence of these isolates. Only a few countries reported, on
voluntary basis, data on specific monitoring on ESBL-/AmpC-/carbapenemases-producing E. coli
and/or on the specific monitoring on carbapenemase-producing microorganisms in 2014, and
according to these data no putative carbapenemase-producer indicator E. coli isolates were identified.
Whereas this initial data is reassuring, carefulness is advisable until a general overview is performed
through specific monitoring in all MSs in 2015 onwards, as required by the legislation. It shall be also
taken into account that the isolation methods applied for the mandatory ESBL-/AmpC-
/carbapenemases-producing E. coli specific monitoring (selective media containing cefotaxime 1 mg/L,
protocol of EURL-AR) would provide a better sensitivity for the selection of ESBL-/AmpC-producers.
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List of abbreviations
% percentage of resistant isolates per category of susceptibility or multiple resistance
%f percentage frequency of isolates tested
% Res percentage of resistant isolates
no data reported
APHA Animal and Plant Health Agency
AMR antimicrobial resistance
AST antimicrobial susceptibility testing
BIOHAZ EFSA Panel on Biological Hazards
CA-SFM French Society for Microbiology
CC clonal complex
CLSI Clinical and Laboratory Standards Institute
CBP clinical breakpoints
CP carbapenemase producer
CTX-M cefotaximase
DD disk diffusion method
DL dilution method
DIN Deutsches Institut fr Normung
EARS-Net European Antimicrobial Resistance Surveillance Network
EC European Commission
ECDC European Centre for Disease Prevention and Control
ECOFF epidemiological cut-off value
EEA European Economic Area
ESBL extended spectrum beta-lactamase
ETEC enterotoxigenic E. coli
EUCAST European Committee on Antimicrobial Susceptibility Testing
EURL-AR EU Reference Laboratory for Antimicrobial Resistance (www.crl-ar.eu)
FWD food- and waterborne diseases and zoonoses
HACCP hazard analysis and critical control point
HPA Health Protection Agency (UK)
I intermediate
IZD inhibition zone diameter
MDR multiple drug resistance
MIC minimum inhibitory concentration
MRSA meticillin-resistant Staphylococcus aureus
MSSA meticillin-susceptible Staphylococcus aureus
MS Member State
NA not applicable
NCP National Control Programme
NRL National Reference Laboratory
Q quantitative
R resistant
res1res9 resistance to one antimicrobial substance/resistance to nine antimicrobial substances
of the common set for Salmonella
S susceptible
SIR susceptible, intermediate, resistant
ST sequence type
TESSy The European Surveillance System
VTEC vero(cyto)toxigenic E. coli
WHO World Health Organization
Antimicrobial substances
AMC amoxicillin/clavulanate
AMP ampicillin
AZM azithromycin
CAZ ceftazidime
CHL chloramphenicol
CIP ciprofloxacin
CLI clindamycin
CST colistin
CTX cefotaxime
ERY erythromycin
FUS fusidic acid
GEN gentamicin
KAN kanamycin
LZD linezolid
MER meropenem
MUP mupirocin
NAL nalidixic acid
QD quinupristin/dalfopristin
RIF rifampicin
SUL sulfonamides
STR streptomycin
SXT sulfamethoxazole
TGC tigecycline
TIA tiamulin
TET tetracycline
TMP trimethoprim
Finland FI
France FR
Germany DE
Greece GR
Hungary HU
Ireland IE
Italy IT
Latvia LV
Lithuania LT
Luxembourg LU
Malta MT
Netherlands NL
Poland PL
Portugal PT
Romania RO
Slovakia SK
Slovenia SI
Spain ES
Sweden SE
United Kingdom UK
Definitions
Antimicrobial-resistant In the case of quantitative data, an isolate was defined as resistant to a
isolate selected antimicrobial when its minimum inhibitory concentration (MIC) value
(in mg/L) was above the cut-off value or the disc diffusion diameter (in mm)
was below the cut-off value. The cut-off values, used to interpret MIC
distributions (mg/L) for bacteria from animals and food, are shown in
Material and methods, Table 5, Table 6 and Table 7.
In the case of qualitative data, an isolate was regarded as resistant when the
country reported it as resistant using its own cut-off value or break point
Level of antimicrobial The percentage of resistant isolates among the tested isolates
resistance
Reporting MS group MSs (MSs) that provided data and were included in the relevant table for
antimicrobial resistance data for the bacteriafood/animal category
antimicrobial combination
Terms used to describe the Rare: < 0.1%
antimicrobial resistance levels
Very low: 0.1% to 1.0%
Low: > 1.0% to 10.0%
Moderate: > 10.0% to 20.0%
1. Summary
Table abbreviation Table name
SUMTABL1 Summary of phenotypic characterisation of third generation cephalosporin resistance in
Salmonella from poultry in 2014
SUMTABL2 Summary of phenotypic characterisation of third generation cephalosporin resistance in
E. coli from poultry in 2014
3.1. Salmonella
COMSALMTURKMEAT Complete susceptibility and MDR in Salmonella spp. from meat from turkeys in 20
14
COMSALMTURK Complete susceptibility and MDR in Salmonella spp. from fattening turkeys in 201
4
COMSTANTURK Complete susceptibility and MDR in Salmonella Stanley from fattening turkeys in 2
014
COMTYPHIBR Complete susceptibility and MDR in Salmonella Typhimurium from broilers in 201
4
COMTYPHILAY Complete susceptibility and MDR in Salmonella Typhimurium from laying hens in 2
014
COMTYPHIPIGMEAT Complete susceptibility and MDR in Salmonella Typhimurium from meat from pigs
in 2014
COMTYPHITURKMEAT Complete susceptibility and MDR in Salmonella Typhimurium from meat from turk
eys in 2014
COMTYPHITURK Complete susceptibility and MDR in Salmonella Typhimurium from fattening turke
ys in 2014
COSALM Co-
resistance to cefotaxime and ciprofloxacin (applying EUCAST clinical breakpoints)
DERBYTURKD Occurrence of resistance to selected antimicrobials,
Panel 1, in Salmonella Derby isolates from fattening turkeys in 2014, using harmo
nised epidemiological cut-off values
ENTERBRD Occurrence of resistance to selected antimicrobials,
Panel 1, in Salmonella Enteritidis isolates from broilers in 2014, using harmonised
epidemiological cut-off values
ENTERBRD2 Occurrence of resistance to selected antimicrobials,
Panel 2, in Salmonella Enteritidis isolates from broilers in 2014, using harmonised
epidemiological cut-off values
ENTERBRMEATD Occurrence of resistance to selected antimicrobials,
Panel 1, in Salmonella Enteritidis from meat from broilers in 2014, using harmonis
ed epidemiological cut-off values
ENTERBRMEATD2 Occurrence of resistance to selected antimicrobials,
Panel 2, in Salmonella Enteritidis from meat from broilers in 2014, using harmonis
ed epidemiological cut-off values
ENTERLAYD Occurrence of resistance to selected antimicrobials,
Panel 1, in Salmonella Enteritidis isolates from laying hens in 2014, using harmoni
sed epidemiological cut-off values
ENTERLAYD2 Occurrence of resistance to selected antimicrobials,
Panel 2, in Salmonella Enteritidis isolates from laying hens in 2014, using harmoni
sed epidemiological cut-off values
ENTEROVERVIEW Overview of countries reporting antimicrobial resistance data using MICs on Salmo
nella Enteritidis from humans and various animal and food categories in 2014
ENTERTURKD Occurrence of resistance to selected antimicrobials,
Panel 1, in Salmonella Enteritidis isolates from fattening turkeys in 2014, using ha
rmonised epidemiological cut-off values
FREQINFBR Frequency distribution of completely susceptible isolates and resistant isolates to f
rom one to nine antimicrobials classes in Salmonella Infantis
from broilers in 2014
FREQKENMBR Frequency distribution of completely susceptible isolates and resistant isolates to f
rom one to nine antimicrobials classes in Salmonella Kentuky
from broilers in 2014
FREQSALMBR Frequency distribution of completely susceptible isolates and resistant isolates to f
rom one to nine antimicrobials classes in Salmonella spp. from broilers in 2014
FREQSALMLAY Frequency distribution of completely susceptible isolates and resistant isolates to f
rom one to nine antimicrobials
classes in Salmonella spp. from laying hens in 2014
HADARTURKD Occurrence of resistance to selected antimicrobials,
Panel 1, in Salmonella Hadar isolates from fattening turkeys in 2014, using harmo
nised epidemiological cut-off values
FIG49 Spatial distribution of nalidixic acid resistance among Salmonella spp. from fattening
turkeys in 2014
FIG50 Spatial distribution of cefotaxime resistance among Salmonella spp. from fattening
turkeys in 2014
FIG51 Frequency distribution of completely susceptible isolates and resistant isolates to one to
nine antimicrobials classes in Salmonella spp. from fattening turkeys in 2014
FIG52 Tigecycline resistance in Salmonella spp.
3.2. Campylobacter
CAMPCOHUM Antimicrobial resistance in Campylobacter coli from humans per country in 2014
CAMPJEHUM Antimicrobial resistance in Campylobacter jejuni from humans per country in 2014
CAMPTRAVHUM Proportion of tested Campylobacter jejuni and C. coli isolates from human cases
associated with travel, domestic cases and cases with unknown travel
information by country in 2014
COMCAMPCOHUM Complete susceptibility, MDR and co-resistance in Campylobacter coli
from humans in 2014
COMCAMPJEHUM Complete susceptibility, MDR and co-resistance in Campylobacter jejuni
from humans in 2014
MM2 Antimicrobials reported, methods used, type of data reported and interpretive criteria
applied by MS for human Campylobacter AST data in 2014
COMESCHETURK Complete susceptibility and MDR in indicator in Escherichia coli from fattening turkeys i
n 2014
ESCHEBR2 Occurrence of resistance to selected antimicrobials, Panel 2, in indicator Escherichia coli
from broilers in MSs reporting data in
2014, using harmonised epidemiological cut-off values
ESCHEBRDESBL2 Specific monitoring of enzyme-producing E. coli from broilers in 2014:
occurrence of resistance to selected antimicrobials,
Panel 2, using harmonised epidemiological cut-off values
ESCHEBRDESBL Specific monitoring of enzyme-producing E. coli from broilers in 2014:
occurrence of resistance to selected antimicrobials,
Panel 1, using harmonised epidemiological cut-off values
ESCHEBRMEATD2 Specific monitoring of enzyme-producing E. coli from broiler meat in 2014:
occurrence of resistance to selected antimicrobials,
Panel 2, using harmonised epidemiological cut-off values
ESCHEBRMEATESBL Specific monitoring of enzyme-producing E. coli from broiler meat in 2014:
occurrence of resistance to selected antimicrobials,
Panel 1, using harmonised epidemiological cut-off values
ESCHEBR Occurrence of resistance to selected antimicrobials, Panel 1, in indicator Escherichia coli
from broilers in MSs reporting data in
2014, using harmonised epidemiological cut-off values
ESCHEMEAT Occurrence of resistance to selected antimicrobials in indicator Escherichia coli from
meat in MSs reporting data in 2014, using harmonised epidemiological cut-
off values
ESCHEOVERVIEWESBL Overview of countries reporting antimicrobial resistance data using MIC on specific
monitoring of enzyme-producing E. coli
from various animal and food categories in 2014
ESCHEOVERVIEW Overview of countries reporting antimicrobial resistance data using MIC on indicator Es
cherichia coli from various animal and food categories in 2014
ESCHETURK2 Occurrence of resistance to selected antimicrobials, Panel 2, in indicator
Escherichia coli isolates from fattening turkeys in 2014, using harmonised epid
emiological cut-off values
ESCHETURKESBL2 Specific monitoring of enzyme-producing E. coli from fattening turkeys in 2014:
occurrence of resistance to selected antimicrobials,
Panel 2, using harmonised epidemiological cut-off values
ESCHETURKESBL Specific monitoring of enzyme-producing E. coli from fattening turkeys in 2014:
occurrence of resistance to selected antimicrobials,
Panel 1, using harmonised epidemiological cut-off values
ESCHETURK Occurrence of resistance to selected antimicrobials, Panel 1, in indicator
Escherichia coli isolates from fattening turkeys in 2014, using harmonised epid
emiological cut-off values
FREQESCHEBR Frequency distribution of completely susceptible isolates and resistant isolates to from
one to eleven antimicrobials in commensal indicator Escherichia coli from broile
rs in 2014
FREQESCHETURK Frequency distribution of completely susceptible isolates and resistant isolates to from
one to eleven antimicrobials in Escherichia coli from fattening turkeys in 2014
MULTIESCHEBR MDR patterns of selected antimicrobials, Panel 1,
in indicator Escherichia coli from broilers in 2014
MULTIESCHETURK MDR patterns of selected antimicrobials, Panel
1, in indicator Escherichia coli from fattening turkeys in 2014
MRSAAMR Occurrence of resistance for selected antimicrobials in MRSA from food and animals in
2014, using harmonised epidemiological cut-off values
MRSAANIMALCLIN MRSA in food-producing animals, clinical investigations, 2014
MRSAOVERVIEW Overview of countries reporting data on MRSA in animals and food in 2014
MULTIMRSABREEDGG MDR patterns of selected antimicrobials in Staphylococcus aureus meticillin resistant fro
m breeding Gallus gallus in 2014
MULTIMRSALH MDR patterns of selected antimicrobials in Staphylococcus aureus meticillin resistant fro
m laying hens in 2014.
3.5.1. Third-generation cephalosporin and carbapenem resistance in Escherichia coli and Salmonella
Table abbreviation Table name
RESCEPH1 Occurrence of resistance to beta-lactam and carbapenem compounds among
Salmonella spp. subject to supplementary testing from broilers, laying hens
and meat from broilers in 2014, using harmonised ECOFFs
RESCEPH2 Resistance phenotypes identified in Salmonella spp. subjected to supplementary testing
from broilers, laying hens and meat from broilers in MSs in 2014
RESCEPH3 Occurrence of resistance to beta-lactam and carbapenem compounds in indicator
E. coli isolates from broiler flocks subject to supplementary testing in 2014, using
harmonised ECOFFs
RESCEPH4 Presumptive ESBL and AmpC phenotypes identified in indicator E. coli isolates from
broiler flocks subjected to supplementary testing in 2014
RESCEPH5 Occurrence of resistance to beta-lactam and carbapenem compounds in indicator
E. coli isolates from fattening turkeys subject to supplementary testing in
2014, using harmonised ECOFFs
RESCEPH6 Presumptive ESBL and AmpC phenotypes identified in indicator E. coli isolates from
fattening turkeys subjected to supplementary testing in 2014
RESCEPH7 Occurrence of resistance to selected antimicrobials in Escherichia coli from broilers and
fattening turkeys in reporting countries, specific ESBL monitoring, Panel 2, in
2014
RESCEPH8 Occurrence of resistance to selected antimicrobials in Escherichia coli from broilers and
fattening turkeys in reporting countries, specific ESBL monitoring, panel 2, in
2014
RESCEPH9 Presumptive ESBL and AmpC phenotypes identified in E. coli from broilers recovered
from the specific monitoring on ESBLs/AmpC/Carbapenemases and subjected
to supplementary testing or molecular typing confirmation in 2014
RESCEPH10 Resistance (%) to cefotaxime and ceftazidime in Salmonella spp. and indicator E. coli
isolates in MSs in 2014 testing both bacterial species in broilers or fattening
turkeys